Purves 15 5/14/04 10:16 AM Page 371 Chapter 15 · Purves 15 5/14/04 10:16 AM Page 374. Figure 15.3...

Overview

Skeletal (striated) muscle contraction is initiated by “lower” motor neuronsin the spinal cord and brainstem. The cell bodies of the lower neurons arelocated in the ventral horn of the spinal cord gray matter and in the motornuclei of the cranial nerves in the brainstem. These neurons (also called αmotor neurons) send axons directly to skeletal muscles via the ventral rootsand spinal peripheral nerves, or via cranial nerves in the case of the brain-stem nuclei. The spatial and temporal patterns of activation of lower motorneurons are determined primarily by local circuits located within the spinalcord and brainstem. Descending pathways from higher centers comprisethe axons of “upper” motor neurons and modulate the activity of lowermotor neurons by influencing this local circuitry. The cell bodies of uppermotor neurons are located either in the cortex or in brainstem centers, suchas the vestibular nucleus, the superior colliculus, and the reticular formation.The axons of the upper motor neurons typically contact the local circuit neu-rons in the brainstem and spinal cord, which, via relatively short axons, con-tact in turn the appropriate combinations of lower motor neurons. The localcircuit neurons also receive direct input from sensory neurons, thus mediat-ing important sensory motor reflexes that operate at the level of the brain-stem and spinal cord. Lower motor neurons, therefore, are the final commonpathway for transmitting neural information from a variety of sources to theskeletal muscles.

Neural Centers Responsible for Movement

The neural circuits responsible for the control of movement can be dividedinto four distinct but highly interactive subsystems, each of which makes aunique contribution to motor control (Figure 15.1). The first of these subsys-tems is the local circuitry within the gray matter of the spinal cord and theanalogous circuitry in the brainstem. The relevant cells include the lowermotor neurons (which send their axons out of the brainstem and spinal cordto innervate the skeletal muscles of the head and body, respectively) and thelocal circuit neurons (which are the major source of synaptic input to thelower motor neurons). All commands for movement, whether reflexive orvoluntary, are ultimately conveyed to the muscles by the activity of thelower motor neurons; thus these neurons comprise, in the words of the greatBritish neurophysiologist Charles Sherrington, the “final common path” formovement. The local circuit neurons receive sensory inputs as well asdescending projections from higher centers. Thus, the circuits they form pro-vide much of the coordination between different muscle groups that is

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Figure 15.1 Overall organization ofneural structures involved in the controlof movement. Four systems—localspinal cord and brainstem circuits,descending modulatory pathways, thecerebellum, and the basal ganglia—make essential and distinct contribu-tions to motor control.

essential for organized movement. Even after the spinal cord is disconnectedfrom the brain in an experimental animal such as a cat, appropriate stimula-tion of local spinal circuits elicits involuntary but highly coordinated limbmovements that resemble walking.

The second motor subsystem consists of the upper motor neurons whosecell bodies lie in the brainstem or cerebral cortex and whose axons descendto synapse with the local circuit neurons or, more rarely, with the lowermotor neurons directly. The upper motor neuron pathways that arise in thecortex are essential for the initiation of voluntary movements and for com-plex spatiotemporal sequences of skilled movements. In particular, descend-ing projections from cortical areas in the frontal lobe, including Brodmann’sarea 4 (the primary motor cortex), the lateral part of area 6 (the lateral pre-motor cortex), and the medial part of area 6 (the medial premotor cortex)are essential for planning, initiating, and directing sequences of voluntarymovements. Upper motor neurons originating in the brainstem are responsi-ble for regulating muscle tone and for orienting the eyes, head, and bodywith respect to vestibular, somatic, auditory, and visual sensory information.Their contributions are thus critical for basic navigational movements, andfor the control of posture.

The third and fourth subsystems are complex circuits with output path-ways that have no direct access to either the local circuit neurons or thelower motor neurons; instead, they control movement by regulating theactivity of the upper motor neurons. The third and larger of these subsys-tems, the cerebellum, is located on the dorsal surface of the pons (see Chap-ter 1). The cerebellum acts via its efferent pathways to the upper motor neu-rons as a servomechanism, detecting the difference, or “motor error,”between an intended movement and the movement actually performed (seeChapter 19). The cerebellum uses this information about discrepancies to

Motor neuron poolsLower motor neurons

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SKELETAL MUSCLES

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postural control

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mediate both real-time and long-term reductions in these motor errors (thelatter being a form of motor learning). As might be expected from thisaccount, patients with cerebellar damage exhibit persistent errors in move-ment. The fourth subsystem, embedded in the depths of the forebrain, con-sists of a group of structures collectively referred to as the basal ganglia (seeChapter 1). The basal ganglia suppress unwanted movements and prepare(or “prime”) upper motor neuron circuits for the initiation of movements.The problems associated with disorders of basal ganglia, such as Parkinson’sdisease and Huntington’s disease, attest to the importance of this complex inthe initiation of voluntary movements (see Chapter 17).

Despite much effort, the sequence of events that leads from volitionalthought to movement is still poorly understood. The picture is clearest, how-ever, at the level of control of the muscles themselves. It therefore makessense to begin an account of motor behavior by considering the anatomicaland physiological relationships between lower motor neurons and the mus-cle fibers they innervate.

Motor Neuron–Muscle Relationships

By injecting individual muscle groups with visible tracers that are trans-ported by the axons of the lower motor neurons back to their cell bodies, thelower motor neurons that innervate each of the body’s skeletal muscles canbe seen in histological sections of the ventral horns of the spinal cord. Eachlower motor neuron innervates muscle fibers within a single muscle, and allthe motor neurons innervating a single muscle (called the motor neuronpool for that muscle) are grouped together into rod-shaped clusters that runparallel to the long axis of the cord for one or more spinal cord segments(Figure 15.2).

An orderly relationship between the location of the motor neuron poolsand the muscles they innervate is evident both along the length of the spinalcord and across the mediolateral dimension of the cord, an arrangement thatin effect provides a spatial map of the body’s musculature. For example, themotor neuron pools that innervate the arm are located in the cervicalenlargement of the cord and those that innervate the leg in the lumbarenlargement (see Chapter 1). The mapping, or topography, of motor neuronpools in the mediolateral dimension can be appreciated in a cross sectionthrough the cervical enlargement (the level illustrated in Figure 15.3). Thus,neurons that innervate the axial musculature (i.e., the postural muscles ofthe trunk) are located medially in the cord. Lateral to these cell groups aremotor neuron pools innervating muscles located progressively more laterallyin the body. Neurons that innervate the muscles of the shoulders (or pelvis,if one were to look at a similar section in the lumbar enlargement; see Figure15.2) are the next most lateral group, whereas those that innervate the proxi-mal muscles of the arm (or leg) are located laterally to these. The motor neu-ron pools that innervate the distal parts of the extremities, the fingers or toes,lie farthest from the midline. This spatial organization provides clues aboutthe functions of the descending upper motor neuron pathways described inthe following chapter; some of these pathways terminate primarily in themedial region of the spinal cord, which is concerned with postural muscles,whereas other pathways terminate more laterally, where they have access tothe lower motor neurons that control movements of the distal parts of thelimbs, such as, the toes and the fingers.

Two types of lower motor neuron are found in these neuronal pools.Small g motor neurons innervate specialized muscle fibers that, in combina-

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tion with the nerve fibers that innervate them, are actually sensory receptorscalled muscle spindles (see Chapter 8). The muscle spindles are embeddedwithin connective tissue capsules in the muscle, and are thus referred to asintrafusal muscle fibers (fusal means capsular). The intrafusal muscle fibersare also innervated by sensory axons that send information to the brain andspinal cord about the length and tension of the muscle. The function of the γmotor neurons is to regulate this sensory input by setting the intrafusal mus-cle fibers to an appropriate length (see the next section). The second type oflower motor neuron, called a motor neurons, innervates the extrafusal mus-cle fibers, which are the striated muscle fibers that actually generate theforces needed for posture and movement.

Although the following discussion focuses on the lower motor neurons inthe spinal cord, comparable sets of motor neurons responsible for the controlof muscles in the head and neck are located in the brainstem. The latter neu-rons are distributed in the eight motor nuclei of the cranial nerves in themedulla, pons, and midbrain (see Appendix A). Somewhat confusingly, butquite appropriately, these motor neurons in the brainstem are also calledlower motor neurons.

(B)(A) (C)

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Figure 15.2 Organization of lowermotor neurons in the ventral horn of thespinal cord demonstrated by labeling oftheir cell bodies following injection of aretrograde tracer in individual muscles.Neurons were identified by placing aretrograde tracer into the medial gas-trocnemius or soleus muscle of the cat.(A) Section through the lumbar level ofthe spinal cord showing the distributionof labeled cell bodies. Lower motor neu-rons form distinct clusters (motor pools)in the ventral horn. Spinal cord crosssections (B) and a reconstruction seenfrom the dorsal surface (C) illustrate thedistribution of motor neurons innervat-ing individual skeletal muscles in bothaxes of the cord. The cylindrical shapeand distinct distribution of differentpools are especially evident in the dor-sal view of the reconstructed cord. Thedashed lines in (C) represent individuallumbar and sacral spinal cord segments.(After Burke et al., 1977.)

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Figure 15.3 Somatotopic organizationof lower motor neurons in a cross sec-tion of the ventral horn at the cervicallevel of the spinal cord. Motor neuronsinnervating axial musculature arelocated medially, whereas those inner-vating the distal musculature arelocated more laterally.

The Motor Unit

Most mature extrafusal skeletal muscle fibers in mammals are innervated byonly a single α motor neuron. Since there are by far more muscle fibers thanmotor neurons, individual motor axons branch within muscles to synapseon many different fibers that are typically distributed over a relatively widearea within the muscle, presumably to ensure that the contractile force of themotor unit is spread evenly (Figure 15.4). In addition, this arrangementreduces the chance that damage to one or a few α motor neurons will signif-icantly alter a muscle’s action. Because an action potential generated by a


Proximalmuscles

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Motor neuronin spinal cord

Muscle fibers innervatedby a single motor neuron

Figure 15.4 The motor unit. (A) Dia-gram showing a lower motor neuron inthe spinal cord and the course of itsaxon to its target muscle. (B) Eachmotor neuron synapses with multiplefibers within the muscle. The motorneuron and the fibers it contacts definethe motor unit. Cross section throughthe muscle shows the relatively diffusedistribution of muscle fibers (red dots)contacted by the motor neuron.

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motor neuron normally brings to threshold all of the muscle fibers it con-tacts, a single α motor neuron and its associated muscle fibers together con-stitute the smallest unit of force that can be activated to produce movement.Sherrington was again the first to recognize this fundamental relationshipbetween an α motor neuron and the muscle fibers it innervates, for which hecoined the term motor unit.

Both motor units and the α motor neurons themselves vary in size. Smallα motor neurons innervate relatively few muscle fibers and form motorunits that generate small forces, whereas large motor neurons innervatelarger, more powerful motor units. Motor units also differ in the types ofmuscle fibers that they innervate. In most skeletal muscles, the smallermotor units comprise small “red” muscle fibers that contract slowly andgenerate relatively small forces; but, because of their rich myoglobin content,plentiful mitochondria, and rich capillary beds, such small red fibers areresistant to fatigue (these units are also innervated by relatively small αmotor neurons). These small units are called slow (S) motor units and areespecially important for activities that require sustained muscular contrac-tion, such as the maintenance of an upright posture. Larger α motor neuronsinnervate larger, pale muscle fibers that generate more force; however, thesefibers have sparse mitochondria and are therefore easily fatigued. Theseunits are called fast fatigable (FF) motor units and are especially importantfor brief exertions that require large forces, such as running or jumping. Athird class of motor units has properties that lie between those of the othertwo. These fast fatigue-resistant (FR) motor units are of intermediate sizeand are not quite as fast as FF units. They generate about twice the force of aslow motor unit and, as the name implies, are substantially more resistant tofatigue (Figure 15.5).

These distinctions among different types of motor units indicate how thenervous system produces movements appropriate for different circum-stances. In most muscles, small, slow motor units have lower thresholds foractivation than the larger units and are tonically active during motor actsthat require sustained effort (standing, for instance). The thresholds for thelarge, fast motor units are reached only when rapid movements requiringgreat force are made, such as jumping. The functional distinctions between

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Figure 15.5 Comparison of the forceand fatigability of the three differenttypes of motor units. In each case, theresponse reflects stimulation of a singlemotor neuron. (A) Change in muscletension in response to a single motorneuron action potential. (B) Tension inresponse to repetitive stimulation of the motor neurons. (C) Response torepeated stimulation at a level thatevokes maximum tension. The ordinaterepresents the force generated by eachstimulus. Note the strikingly differentfatigue rates. (After Burke et al., 1974.)

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the various classes of motor units also explain some structural differencesamong muscle groups. For example, a motor unit in the soleus (a muscleimportant for posture that comprises mostly small, slow units) has an aver-age innervation ratio of 180 muscle fibers for each motor neuron. In contrast,the gastrocnemius, a muscle that comprises both small and larger units, hasan innervation ratio of ~1000–2000 muscle fibers per motor neuron, and cangenerate forces needed for sudden changes in body position. More subtlevariations are present in athletes on different training regimens. Thus, mus-cle biopsies show that sprinters have a larger proportion of powerful butrapidly fatiguing pale fibers in their leg muscles than do marathoners. Otherdifferences are related to the highly specialized functions of particular mus-cles. For instance, the eyes require rapid, precise movements but littlestrength; in consequence, extraocular muscle motor units are extremelysmall (with an average innervation ratio of only 3!) and have a very high pro-portion of muscle fibers capable of contracting with maximal velocity.

The Regulation of Muscle Force

Increasing or decreasing the number of motor units active at any one timechanges the amount of force produced by a muscle. In the 1960s, ElwoodHenneman and his colleagues at Harvard Medical School found that pro-gressive increases in muscle tension could be produced by progressivelyincreasing the activity of axons that provide input to the relevant pool oflower motor neurons. This gradual increase in tension results from therecruitment of motor units in a fixed order according to their size. By stimu-lating either sensory nerves or upper motor pathways that project to a lowermotor neuron pool while measuring the tension changes in the muscle, Hen-neman found that in experimental animals only the smallest motor units inthe pool are activated by weak synaptic stimulation. When synaptic inputincreases, progressively larger motor units that generate larger forces arerecruited: As the synaptic activity driving a motor neuron pool increases,low threshold S units are recruited first, then FR units, and finally, at thehighest levels of activity, the FF units. Since these original experiments, evi-dence for the orderly recruitment of motor units has been found in a varietyof voluntary and reflexive movements. As a result, this systematic relation-ship has come to be known as the size principle.

An illustration of how the size principle operates for the motor units ofthe medial gastrocnemius muscle in the cat is shown in Figure 15.6. Whenthe animal is standing quietly, the force measured directly from the muscletendon is only a small fraction (about 5%) of the total force that the musclecan generate. The force is provided by the S motor units, which make upabout 25% of the motor units in this muscle. When the cat begins to walk,larger forces are necessary: locomotor activities that range from slow walk-ing to fast running require up to 25% of the muscle’s total force capacity.This additional need is met by the recruitment of FR units. Only movementssuch as galloping and jumping, which are performed infrequently and forshort periods, require the full power of the muscle; such demands are metby the recruitment of the FF units. Thus, the size principle provides a simplesolution to the problem of grading muscle force: The combination of motorunits activated by such orderly recruitment optimally matches the physio-logical properties of different motor unit types with the range of forcesrequired to perform different motor tasks.

The frequency of the action potentials generated by motor neurons alsocontributes to the regulation of muscle tension. The increase in force that


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Figure 15.6 The recruitment of motorneurons in the cat medial gastrocne-mius muscle under different behavioralconditions. Slow (S) motor units pro-vide the tension required for standing.Fast fatigue-resistant (FR) units providethe additional force needed for walkingand running. Fast fatigable (FF) unitsare recruited for the most strenuousactivities, such as jumping. (After Walmsley et al., 1978.)

occurs with increased firing rate reflects the summation of successive musclecontractions: The muscle fibers are activated by the next action potentialbefore they have had time to completely relax, and the forces generated bythe temporally overlapping contractions are summed (Figure 15.7). The low-est firing rates during a voluntary movement are on the order of 8 per sec-ond (Figure 15.8). As the firing rate of individual units rises to a maximumof about 20–25 per second in the muscle being studied here, the amount offorce produced increases. At the highest firing rates, individual muscle fibersare in a state of “fused tetanus”—that is, the tension produced in individualmotor units no longer has peaks and troughs that correspond to the individ-ual twitches evoked by the motor neuron’s action potentials. Under normalconditions, the maximum firing rate of motor neurons is less than thatrequired for fused tetanus (see Figure 15.8). However, the asynchronous fir-ing of different lower motor neurons provides a steady level of input to themuscle, which causes the contraction of a relatively constant number ofmotor units and averages out the changes in tension due to contractions andrelaxations of individual motor units. All this allows the resulting move-ments to be executed smoothly.

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Figure 15.7 The effect of stimulationrate on muscle tension. (A) At low fre-quencies of stimulation, each actionpotential in the motor neuron results ina single twitch of the related musclefibers. (B) At higher frequencies, thetwitches sum to produce a force greaterthan that produced by single twitches.(C) At a still higher frequency of stimu-lation, the force produced is greater, butindividual twitches are still apparent.This response is referred to as unfusedtetanus. (D) At the highest rates ofmotor neuron activation, individualtwitches are no longer apparent (a con-dition called fused tetanus).

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Figure 15.8 Motor units recordedtranscutaneously in a muscle of thehuman hand as the amount of volun-tary force produced is progressivelyincreased. Motor units (represented bythe lines between the dots) are initiallyrecruited at a low frequency of firing (8 Hz); the rate of firing for each unitincreases as the subject generates moreand more force. (After Monster andChan, 1977.)

The Spinal Cord Circuitry Underlying Muscle Stretch Reflexes

The local circuitry within the spinal cord mediates a number of sensorymotor reflex actions. The simplest of these reflex arcs entails a sensoryresponse to muscle stretch, which provides direct excitatory feedback to themotor neurons innervating the muscle that has been stretched (Figure 15.9).As already mentioned, the sensory signal for the stretch reflex originates inmuscle spindles, the sensory receptors embedded within most muscles (seethe previous section and Chapter 8). The spindles comprise 8–10 intrafusalfibers arranged in parallel with the extrafusal fibers that make up the bulk ofthe muscle (Figure 15.9A). Large-diameter sensory fibers, called Ia afferents,are coiled around the central part of the spindle. These afferents are thelargest axons in peripheral nerves and, since action potential conductionvelocity is a direct function of axon diameter (see Chapters 2 and 3), theymediate very rapid reflex adjustments when the muscle is stretched. Thestretch imposed on the muscle deforms the intrafusal muscle fibers, which inturn initiate action potentials by activating mechanically gated ion channelsin the afferent axons coiled around the spindle. The centrally projectingbranch of the sensory neuron forms monosynaptic excitatory connectionswith the α motor neurons in the ventral horn of the spinal cord that innervatethe same (homonymous) muscle and, via local circuit neurons, formsinhibitory connections with the α motor neurons of antagonistic (heterony-mous) muscles. This arrangement is an example of what is called reciprocalinnervation and results in rapid contraction of the stretched muscle and simul-taneous relaxation of the antagonist muscle. All of this leads to especiallyrapid and efficient responses to changes in the length or tension in the muscle(Figure 15.9B). The excitatory pathway from a spindle to the α motor neuronsinnervating the same muscle is unusual in that it is a monosynaptic reflex; inmost cases, sensory neurons from the periphery do not contact the lowermotor neuron directly but exert their effects through local circuit neurons.

This monosynaptic reflex arc is variously referred to as the “stretch,”“deep tendon,” or “myotatic” reflex, and it is the basis of the knee, ankle,jaw, biceps, or triceps responses tested in a routine neurological examination.The tap of the reflex hammer on the tendon stretches the muscle and there-fore excites an afferent volley of activity in the Ia sensory axons that inner-vate the muscle spindles. The afferent volley is relayed to the α motor neu-rons in the brainstem or spinal cord, and an efferent volley returns to themuscle (see Figure 1.5). Since muscles are always under some degree of


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stretch, this reflex circuit is normally responsible for the steady level of ten-sion in muscles called muscle tone. Changes in muscle tone occur in a vari-ety of pathological conditions, and it is these changes that are assessed byexamination of tendon reflexes.

In terms of engineering principles, the stretch reflex arc is a negative feed-back loop used to maintain muscle length at a desired value (Figure 15.9C).The appropriate muscle length is specified by the activity of descendingupper motor neuron pathways that influence the motor neuron pool. Devia-tions from the desired length are detected by the muscle spindles, sinceincreases or decreases in the stretch of the intrafusal fibers alter the level ofactivity in the sensory axons that innervate the spindles. These changes leadin turn to adjustments in the activity of the α motor neurons, returning themuscle to the desired length by contracting the stretched muscle and relax-ing the opposed muscle group, and by restoring the level of spindle activityto what it was before.

The smaller γ motor neurons control the functional characteristics of themuscle spindles by modulating their level of excitability. As was describedearlier, when the muscle is stretched, the spindle is also stretched and therate of discharge in the afferent fibers increased. When the muscle shortens,however, the spindle is relieved of tension, or “unloaded,” and the sensoryaxons that innervate the spindle might therefore be expected to fall silentduring contraction. However, they remain active. The γ motor neurons ter-minate on the contractile poles of the intrafusal fibers, and the activation ofthese neurons causes intrafusal fiber contraction—in this way maintainingthe tension on the middle (or equatorial region) of the intrafusal fiberswhere the sensory axons terminate. Thus, co-activation of the α and γ motorneurons allows spindles to function (i.e., send information centrally) at allmuscle lengths during movements and postural adjustments.

The Influence of Sensory Activity on Motor Behavior

The level of γ motor neuron activity often is referred to as γ bias, or gain, andcan be adjusted by upper motor neuron pathways as well as by local reflexcircuitry. The larger the gain of the stretch reflex, the greater the change inmuscle force that results from a given amount of stretch applied to the intra-fusal fibers. If the gain of the reflex is high, then a small amount of stretchapplied to the intrafusal fibers will produce a large increase in the number ofα motor neurons recruited and a large increase in their firing rates; this inturn leads to a large increase in the amount of tension produced by theextrafusal fibers. If the gain is low, a greater stretch is required to generatethe same amount of tension in the extrafusal muscle fibers. In fact, the gainof the stretch reflex is continuously adjusted to meet different functionalrequirements. For example, while standing in a moving bus, the gain of thestretch reflex can be modulated by upper motor neuron pathways to com-


Figure 15.9 Stretch reflex circuitry. (A) Diagram of muscle spindle, the sensoryreceptor that initiates the stretch reflex. (B) Stretching a muscle spindle leads toincreased activity in Ia afferents and an increase in the activity of α motor neuronsthat innervate the same muscle. Ia afferents also excite the motor neurons thatinnervate synergistic muscles, and inhibit the motor neurons that innervate antago-nists (see also Figure 1.5). (C) The stretch reflex operates as a negative feedbackloop to regulate muscle length.

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pensate for the variable changes that occur as the bus stops and starts or pro-gresses relatively smoothly. During voluntary movements, α and γ motorneurons are often co-activated by higher centers to prevent muscle spindlesfrom being unloaded (Figure 15.10).

In addition, the level of γ motor neuron activity can be modulated inde-pendently of α activity if the context of a movement requires it. In general,the baseline activity level of γ motor neurons is high if a movement is rela-tively difficult and demands rapid and precise execution. For example,recordings from cat hindlimb muscles show that γ activity is high when theanimal has to perform a difficult movement such as walking across a narrowbeam. Unpredictable conditions, as when the animal is picked up or han-dled, also lead to marked increases in γ activity and greatly increased spin-dle responsiveness.

Gamma motor neuron activity, however, is not the only factor that sets thegain of the stretch reflex. The gain also depends on the level of excitability ofthe α motor neurons that serve as the efferent side of this reflex loop. Thus,in addition to the influence of descending upper motor neuron projections,other local circuits in the spinal cord can change the gain of the stretch reflexby excitation or inhibition of either α or γ motor neurons.

Other Sensory Feedback That Affects Motor Performance

Another sensory receptor that is important in the reflex regulation of motorunit activity is the Golgi tendon organ. Golgi tendon organs are encapsu-

(A) α Motor neuron activation without γ (B) α Motor neuron activation with γ

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Figure 15.10 The role of γ motor neu-ron activity in regulating the responsesof muscle spindles. (A) When α motorneurons are stimulated without activa-tion of γ motor neurons, the response ofthe Ia fiber decreases as the muscle con-tracts. (B) When both α and γ motorneurons are activated, there is nodecrease in Ia firing during muscleshortening. Thus, the γ motor neuronscan regulate the gain of muscle spindlesso they can operate efficiently at anylength of the parent muscle. (After Huntand Kuffler, 1951.)

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lated afferent nerve endings located at the junction of a muscle and tendon(Figure 15.11A; see also Table 9.1). Each tendon organ is innervated by a sin-gle group Ib sensory axon (the Ib axons are slightly smaller than the Ia axonsthat innervate the muscle spindles). In contrast to the parallel arrangementof extrafusal muscle fibers and spindles, Golgi tendon organs are in serieswith the extrafusal muscle fibers. When a muscle is passively stretched, mostof the change in length occurs in the muscle fibers, since they are more elas-


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Figure 15.11 Comparison of the functionof muscle spindles and Golgi tendon organs.(A) Golgi tendon organs are arranged inseries with extrafusal muscle fibers becauseof their location at the junction of muscleand tendon. (B) The two types of musclereceptors, the muscle spindles (1) and theGolgi tendon organs (2), have differentresponses to passive muscle stretch (top) andactive muscle contraction (bottom). Bothafferents discharge in response to passivelystretching the muscle, although the Golgitendon organ discharge is much less thanthat of the spindle. When the extrafusalmuscle fibers are made to contract by stimu-lation of their motor neurons, however, thespindle is unloaded and therefore fallssilent, whereas the rate of Golgi tendonorgan firing increases. (B after Patton, 1965.)

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Box ALocomotion in the Leech and the LampreyAll animals must coordinate body move-ments so they can navigate successfullyin their environment. All vertebrates,including mammals, use local circuits inthe spinal cord (central pattern genera-tors) to control the coordinated move-ments associated with locomotion. Thecellular basis of organized locomotoractivity, however, has been most thor-oughly studied in an invertebrate, theleech, and a simple vertebrate, the lamprey.

Both the leech and the lamprey lackperipheral appendages for locomotionpossessed by many vertebrates (limbs,flippers, fins, or their equivalent). Fur-thermore, their bodies comprise repeat-ing muscle segments (as well as repeat-ing skeletal elements in the lamprey).Thus, in order to move through thewater, both animals must coordinate themovement of each segment. They do thisby orchestrating a sinusoidal displace-

ment of each body segment in sequence,so that the animal is propelled forwardthrough the water.

The leech is particularly well-suitedfor studying the circuit basis of coordi-nated movement. The nervous system inthe leech consists of a series of intercon-nected segmental ganglia, each withmotor neurons that innervate the corre-sponding segmental muscles (Figure A).These segmental ganglia facilitate elec-trophysiological studies, because there isa limited number of neurons in each andeach neuron has a distinct identity. Theneurons can thus be recognized andstudied from animal to animal, and theirelectrical activity correlated with thesinusoidal swimming movements.

A central pattern generator circuitcoordinates this undulating motion. Inthe leech, the relevant neural circuit is anensemble of sensory neurons, interneu-rons, and motor neurons repeated in each

segmental ganglion that controls the localsequence of contraction and relaxation ineach segment of the body wall muscula-ture (Figure B). The sensory neuronsdetect the stretching and contraction ofthe body wall associated with the se-quential swimming movements. Dorsaland ventral motor neurons in the circuitprovide innervation to dorsal and ventralmuscles, whose phasic contractions propel the leech forward. Sensory infor-mation and motor neuron signals arecoordinated by interneurons that firerhythmically, setting up phasic patternsof activity in the dorsal and ventral cellsthat lead to sinusoidal movement. Theintrinsic swimming rhythm is establishedby a variety of membrane conductancesthat mediate periodic bursts of supra-threshold action potentials followed bywell-defined periods of hyperpolarization.

The lamprey, one of the simplest ver-tebrates, is distinguished by its clearly

Dorsalmuscle

Ventral muscle

Flattenermuscle

Posterior sucker

EMGV

EMGD

Ventralcell

Dorsalcell

Head

(B) LEECH(A) LEECH

Segmental ganglion

To muscles

(A) The leech propels itself through the water by sequential contraction and relaxation of thebody wall musculature of each segment. The segmental ganglia in the ventral midline coordi-nate swimming, each ganglion containing a population of identified neurons. (B) Electricalrecordings from the ventral (EMGV) and dorsal (EMGD) muscles in the leech and the corre-sponding motor neurons show a reciprocal pattern of excitation for the dorsal and ventralmuscles of a given segment.

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segmented musculature and by its lackof bilateral fins or other appendages. Inorder to move through the water, thelamprey contracts and relaxes each mus-cle segment in sequence (Figure C),which produces a sinusoidal motion,much like that of the leech. Again, a cen-tral pattern generator coordinates thissinusoidal movement.

Unlike the leech with its segmentalganglia, the lamprey has a continuousspinal cord that innervates its musclesegments. The lamprey spinal cord issimpler than that of other vertebrates,and several classes of identified neuronsoccupy stereotyped positions. Thisorderly arrangement again facilitates theidentification and analysis of neuronsthat constitute the central pattern genera-tor circuit.

In the lamprey spinal cord, the intrin-sic firing pattern of a set of intercon-nected sensory neurons, interneuronsand motor neurons establishes the pat-tern of undulating muscle contractionsthat underlie swimming (Figure D). Thepatterns of connectivity between neu-rons, the neurotransmitters used by eachclass of cell, and the physiological prop-erties of the elements in the lamprey pat-tern generator are now known. Differentneurons in the circuit fire with distinctrhythmicity, thus controlling specificaspects of the swim cycle (Figure E). Par-ticularly important are reciprocal inhib-itory connections across the midline thatcoordinate the pattern generating cir-cuitry on each side of the spinal cord.This circuitry in the lamprey thus pro-vides a basis for understanding the cir-

cuits that control locomotion in morecomplex vertebrates.

These observations on pattern gener-ating circuits for locomotion in relativelysimple animals have stimulated parallelstudies of terrestrial mammals in whichcentral pattern generators in the spinalcord also coordinate locomotion.Although different in detail, terrestriallocomotion ultimately relies on thesequential movements similar to thosethat propel the leech and the lampreythrough aquatic environments, andintrinsic physiological properties ofspinal cord neurons that establish ryth-micity for coordinated movement.

ReferencesGRILLNER, S., D. PARKER AND A. EL MANIRA

(1998) Vertebrate locomotion: A lamprey per-spective. Ann. N.Y. Acad. Sci. 860: 1–18.MARDER, E. AND R. M. CALABRESE (1996) Prin-ciples of rhythmic motor pattern generation.Physiol. Rev. 76: 687–717.STENT, G. S., W. B. KRISTAN, W. O. FRIESEN, C.A. ORT, M. POON AND R. M. CALABRESE (1978)Neural generation of the leech swimmingmovement. Science 200: 1348–1357.

Record

Record

Midline

EV IV

MV LV

EDID

MDLD

Ventral root Dorsal root

Sensory inputs

Sensory inputs

Brainstem inputs(D) LAMPREY

(C) In the lamprey, as this diagram indicates,the pattern of activity across segments is alsohighly coordinated. (D) The elements of thecentral pattern generator in the lampreyhave been worked out in detail, providing aguide to understanding homologous cir-cuitry in more complex spinal cords.(E) As in the leech, different patterns of elec-trical activity in lamprey spinal neurons(neurons ED and LV in this example) corre-spond to distinct periods in the sequence ofmuscle contractions related to the swimcycle.

LV

ED

(E) LAMPREY

Duration of EMGactivity in each segmental muscle

1 swim cycle

Anterior

Posterior

(C) LAMPREY

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tic than the fibrils of the tendon. When a muscle actively contracts, however,the force acts directly on the tendon, leading to an increase in the tension ofthe collagen fibrils in the tendon organ and compression of the intertwinedsensory receptors. As a result, Golgi tendon organs are exquisitely sensitiveto increases in muscle tension that arise from muscle contraction but, unlikespindles, are relatively insensitive to passive stretch (Figure 15.11B).

The Ib axons from Golgi tendon organs contact inhibitory local circuitneurons in the spinal cord (called Ib inhibitory interneurons) that synapse, inturn, with the α motor neurons that innervate the same muscle. The Golgitendon circuit is thus a negative feedback system that regulates muscle ten-sion; it decreases the activation of a muscle when exceptionally large forcesare generated and this way protects the muscle. This reflex circuit also oper-ates at reduced levels of muscle force, counteracting small changes in muscletension by increasing or decreasing the inhibition of α motor neurons. Underthese conditions, the Golgi tendon system tends to maintain a steady level offorce, counteracting effects that diminish muscle force (such as fatigue). Inshort, the muscle spindle system is a feedback system that monitors andmaintains muscle length, and the Golgi tendon system is a feedback systemthat monitors and maintains muscle force.

Like the muscle spindle system, the Golgi tendon organ system is not aclosed loop. The Ib inhibitory interneurons also receive synaptic inputs froma variety of other sources, including cutaneous receptors, joint receptors,muscle spindles, and descending upper motor neuron pathways (Figure15.12). Acting in concert, these inputs regulate the responsiveness of Ibinterneurons to activity arising in Golgi tendon organs.

Figure 15.12 Negative feedback regula-tion of muscle tension by Golgi tendonorgans. The Ib afferents from tendonorgans contact inhibitory interneurons thatdecrease the activity of α motor neuronsinnervating the same muscle. The Ibinhibitory interneurons also receive inputfrom other sensory fibers, as well as fromdescending pathways. This arrangementprevents muscles from generating exces-sive tension.

Descendingpathways

Ib afferent

Motorneuron

Flexormuscle

Extensormuscle

Golgi tendonorgan

Ib inhibitoryinterneuron

+

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Flexion Reflex Pathways So far, the discussion has focused on reflexes driven by sensory receptorslocated within muscles or tendons. Other reflex circuitry mediates the with-drawal of a limb from a painful stimulus, such as a pinprick or the heat of aflame. Contrary to what might be imagined given the speed with which weare able to withdraw from a painful stimulus, this flexion reflex involvesseveral synaptic links (Figure 15.13). As a result of activity in this circuitry,stimulation of nociceptive sensory fibers leads to withdrawal of the limbfrom the source of pain by excitation of ipsilateral flexor muscles and recip-rocal inhibition of ipsilateral extensor muscles. Flexion of the stimulatedlimb is also accompanied by an opposite reaction in the contralateral limb(i.e., the contralateral extensor muscles are excited while flexor muscles areinhibited). This crossed extension reflex provides postural support duringwithdrawal of the affected limb from the painful stimulus.

Like the other reflex pathways, local circuit neurons in the flexion reflexpathway receive converging inputs from several different sources, includingother spinal cord interneurons and upper motor neuron pathways. Althoughthe functional significance of this complex pattern of connectivity is unclear,changes in the character of the reflex following damage to descending path-ways provides some insight. Under normal conditions, a noxious stimulus isrequired to evoke the flexion reflex; following damage to descending path-ways, however, other types of stimulation, such as squeezing a limb, cansometimes produce the same response. This observation suggests that thedescending projections to the spinal cord modulate the responsiveness of thelocal circuitry to a variety of sensory inputs.

Spinal Cord Circuitry and Locomotion

The contribution of local circuitry to motor control is not, of course, limited toreflexive responses to sensory inputs. Studies of rhythmic movements such aslocomotion and swimming in animal models (Box A) have demonstrated thatlocal circuits in the spinal cord called central pattern generators are fullycapable of controlling the timing and coordination of such complex patternsof movement, and of adjusting them in response to altered circumstances(Box B).

A good example is locomotion (walking, running, etc.). The movement of asingle limb during locomotion can be thought of as a cycle consisting of twophases: a stance phase, during which the limb is extended and placed in contactwith the ground to propel humans or other bipeds forward; and a swing phase,during which the limb is flexed to leave the ground and then brought forwardto begin the next stance phase (Figure 15.14A). Increases in the speed of loco-motion reduce the amount of time it takes to complete a cycle, and most of thechange in cycle time is due to shortening the stance phase; the swing phaseremains relatively constant over a wide range of locomotor speeds.

In quadrupeds, changes in locomotor speed are also accompanied bychanges in the sequence of limb movements. At low speeds, for example,there is a back-to-front progression of leg movements, first on one side andthen on the other. As the speed increases to a trot, the movements of theright forelimb and left hindlimb are synchronized (as are the movements ofthe left forelimb and right hindlimb). At the highest speeds (gallop), themovements of the two front legs are synchronized, as are the movements ofthe two hindlimbs (Figure 15.14B).

Given the precise timing of the movement of individual limbs and thecoordination among limbs that are required in this process, it is natural to


Figure 15.13 Spinal cord circuitryresponsible for the flexion reflex. Stimu-lation of cutaneous receptors in the foot(by stepping on a tack in this example)leads to activation of spinal cord localcircuits that withdraw (flex) the stimu-lated extremity and extend the otherextremity to provide compensatory support.

Cutaneousreceptor

Flexormuscle

Extensormuscle

Extensormuscle

Motorneuron

Cutaneous afferent fiberfrom nociceptor (Aδ)

Stimulated legflexes to withdraw

Opposite legextends to

support

++

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Box BThe Autonomy of Central Pattern Generators:Evidence from the Lobster Stomatogastric GanglionA principle that has emerged from stud-ies of central pattern generators is thatrhythmic patterns of firing elicit complexmotor responses without need of ongo-ing sensory stimulation. A good exampleis the behavior mediated by a smallgroup of nerve cells in lobsters and othercrustaceans called the stomatogastricganglion (STG) that controls the musclesof the gut (Figure A). This ensemble of 30motor neurons and interneurons in thelobster is perhaps the most completelycharacterized neural circuit known. Ofthe 30 cells, defined subsets are essentialfor two distinct rhythmic movements:gastric mill movements that mediategrinding of food by “teeth” in the lob-ster’s foregut, and pyloric movementsthat propel food into the hindgut. Phasicfiring patterns of the motor neurons andinterneurons of the STG are directly cor-related with these two rhythmic move-

ments. Each of the relevant cells has nowbeen identified based on its position inthe ganglion, and its electrophysiologicaland neuropharmacological propertiescharacterized (Figures B and C).

Patterned activity in the motor neu-rons and interneurons of the ganglionbegins only if the appropriate neuromod-ulatory input is provided by sensoryaxons that originate in other ganglia.Depending upon the activity of the sen-sory axons, neuronal ensembles in theSTG produce one of several characteristicrhythmic firing patterns. Once activated,however, the intrinsic membrane proper-ties of identified cells within the ensem-ble sustain the rhythmicity of the circuitin the absence of further sensory input.

Another key fact that has emergedfrom this work is that the same neuronscan participate in different programmedmotor activities, as circumstances

(A) Somatogastric ganglion

Cardiac sac

Brain

Esophagealganglion

Esophagus

Commissuralganglion

Pyloric dilatormuscle

Constrictor muscles

Pylorus

Dorsal dilatormuscle

Gastricmill

Motor nerve

(A) Location of the lobster stomatogastric ganglion in relation to the gut.(B) Subset of identified neurons in the stomatogastric ganglion that generates gastric mill andpyloric activity. The abbreviations indicate individual identified neurons, all of which projectto different pyloric muscles (except the AB neuron, which is an interneuron).(C) Recording from one of the neurons, the lateral pyloric or LP neuron, in this circuit show-ing the different patterns of activity elicited by several neuromodulators known to beinvolved in the normal synaptic interactions in this ganglion.

Control

Dopamine

Proctolin

Serotonin

Pilocarpine

AB PD

VD

IC

PY LP

(B)

(C) Record

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assume that locomotion is accomplished by higher centers that organize thespatial and temporal activity patterns of the individual limbs. However, fol-lowing transection of the spinal cord at the thoracic level, a cat’s hindlimbswill still make coordinated locomotor movements if the animal is supportedand placed on a moving treadmill (Figure 15.14C). Under these conditions,the speed of locomotor movements is determined by the speed of the tread-mill, suggesting that the movement is nothing more than a reflexiveresponse to stretching the limb muscles. This possibility is ruled out, how-ever, by experiments in which the dorsal roots are also sectioned. Althoughthe speed of walking is slowed and the movements are less coordinated thanunder normal conditions, appropriate locomotor movements are stillobserved. These and other observations in experimental animals show thatthe basic rhythmic patterns of limb movement during locomotion are notdependent on sensory input; nor are they dependent on input fromdescending projections from higher centers. Rather, each limb appears tohave its own central pattern generator responsible for the alternating flexionand extension of the limb during locomotion (see Box B). Under normal con-ditions, the central pattern generators for the limbs are variably coupled toeach other by additional local circuits in order to achieve the differentsequences of movements that occur at different speeds.

Although some locomotor movements can also be elicited in humans fol-lowing damage to descending pathways, these are considerably less effectivethan the movements seen in the cat. The reduced ability of the transectedspinal cord to mediate rhythmic stepping movements in humans presum-ably reflects an increased dependence of local circuitry on upper motor neu-ron pathways. Perhaps bipedal locomotion carries with it requirements forpostural control greater than can be accommodated by spinal cord circuitryalone. Whatever the explanation, the basic oscillatory circuits that controlsuch rhythmic behaviors as flying, walking, and swimming in many animalsalso play an important part in human locomotion.

The Lower Motor Neuron Syndrome

The complex of signs and symptoms that arise from damage to the lowermotor neurons of the brainstem and spinal cord is referred to as the “lowermotor neuron syndrome.” In clinical neurology, this constellation of prob-lems must be distinguished from the “upper motor neuron syndrome” thatresults from damage to the descending upper motor neuron pathways (seeChapter 16 for a discussion of the signs and symptoms associated with dam-age to upper motor neurons).


demand. For example, the subset of neu-rons producing gastric mill activity over-laps the subset that generates pyloricactivity. This economic use of neuronalsubsets has not yet been described in thecentral pattern generators of mammals,but seems likely to be a feature of allsuch circuits.

ReferencesHARTLINE, D. K. AND D. M. MAYNARD (1975)Motor patterns in the stomatogastric gan-glion of the lobster, Panulirus argus. J. Exp.Biol. 62: 405–420.MARDER, E. AND R. M. CALABRESE (1996) Prin-ciples of rhythmic motor pattern generation.Physiol. Rev. 76: 687–717.

SELVERSTON, A. I., D. F. RUSSELL AND J. P.MILLER (1976) The stomatogastric nervoussystem: Structure and function of a smallneural network. Progress in Neurobiology 7:215–290.

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Damage to lower motor neuron cell bodies or their peripheral axonsresults in paralysis (loss of movement) or paresis (weakness) of the affectedmuscles, depending on the extent of the damage. In addition to paralysisand/or paresis, the lower motor neuron syndrome includes a loss of reflexes(areflexia) due to interruption of the efferent (motor) limb of the sensorymotor reflex arcs. Damage to lower motor neurons also entails a loss of mus-cle tone, since tone is in part dependent on the monosynaptic reflex arc thatlinks the muscle spindles to the lower motor neurons (see also Box D inChapter 16). A somewhat later effect is atrophy of the affected muscles dueto denervation and disuse. The muscles involved may also exhibit fibrilla-tions and fasciculations, which are spontaneous twitches characteristic ofsingle denervated muscle fibers or motor units, respectively. These phenom-ena arise from changes in the excitability of denervated muscle fibers in thecase of fibrillation, and from abnormal activity of injured α motor neurons inthe case of fasciculations. These spontaneous contractions can be readily rec-ognized in an electromyogram, providing an especially helpful clinical toolin diagnosing lower motor neuron disorders (Box C).

Swing Stance(A)

(B)

(C)LH

FlexorsEMG

WALK

LFRHRF

LHTROT

LFRHRF

LHPACE

LFRHRF

LHGALLOP

LFRHRF

Time

Extensors

LH LFRH RF

FE3 E1 E2 E3 F

Stance

Extensors

Flexors

Swing

Level of transectionof spinal cord

Flexion Extension

Figure 15.14 The cycle of locomotionfor terrestrial mammals (a cat in thisinstance) is organized by central patterngenerators. (A) The step cycle, showingleg flexion (F) and extension (E) andtheir relation to the swing and stancephases of locomotion. EMG indicateselectromyographic recordings. (B) Com-parison of the stepping movements fordifferent gaits. Brown bars, foot lifted(swing phase); gray bars, foot planted(stance phase). (C) Transection of thespinal cord at the thoracic level isolatesthe hindlimb segments of the cord. Thehindlimbs are still able to walk on atreadmill after recovery from surgery,and reciprocal bursts of electrical activ-ity can be recorded from flexors duringthe swing phase and from extensorsduring the stance phase of walking.(After Pearson, 1976.)

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Summary

Four distinct but highly interactive motor subsystems—local circuits in thespinal cord and brainstem, descending upper motor neuron pathways thatcontrol these circuits, the basal ganglia, and the cerebellum—all make essen-tial contributions to motor control. Alpha motor neurons located in thespinal cord and in the cranial nerve nuclei in the brainstem directly link thenervous system and muscles, with each motor neuron and its associatedmuscle fibers constituting a functional entity called the motor unit. Motorunits vary in size, amount of tension produced, speed of contraction, anddegree of fatigability. Graded increases in muscle tension are mediated byboth the orderly recruitment of different types of motor units and anincrease in motor neuron firing frequency. Local circuitry involving sensoryinputs, local circuit neurons, and α and γ motor neurons are especiallyimportant in the reflexive control of muscle activity. The stretch reflex is amonosynaptic circuit with connections between sensory fibers arising frommuscle spindles and the α motor neurons that innervate the same or syner-


Box CAmyotrophic Lateral SclerosisAmyotrophic lateral sclerosis (ALS) is aneurodegenerative disease that affects anestimated 0.05% of the population in theUnited States. It is also called LouGehrig’s disease, after the New YorkYankees baseball player who died of thedisorder in 1936. ALS is characterized bythe slow but inexorable degeneration ofα motor neurons in the ventral horn ofthe spinal cord and brainstem (lowermotor neurons), and of neurons in themotor cortex (upper motor neurons).Affected individuals show progressiveweakness due to upper and/or lowermotor neuron involvement, wasting ofskeletal muscles due to lower motor neu-ron involvement, and usually die within5 years of onset. Sadly, these patients arecondemned to watch their own demise,since the intellect remains intact. Noavailable therapy effectively prevents theinexorable progression of this disease.

Approximately 10% of ALS cases arefamilial, and several distinct familialforms have been identified. An autoso-mal dominant form of familial ALS(FALS) is caused by mutations of the

gene that encodes the cytosolic antioxi-dant enzyme copper/zinc superoxidedismutase (SOD1). Mutations of SOD1account for roughly 20% of families withFALS. A rare autosomal recessive, juve-nile-onset form is caused by mutations ina protein called alsin, a putative GTPaseregulator. Another rare type of FALSconsists of a slowly progressive, autoso-mal dominant, lower motor neuron dis-ease without sensory symptoms, withonset in early adulthood; this form iscaused by mutations of a protein nameddynactin.

How these mutant genes lead to thephenotype of motor neuron disease isuncertain. Defects of axonal transporthave long been hypothesized to causeALS. Evidence for this cause is that trans-genic mice with mutant SOD1 exhibitdefects in slow axonal transport early inthe course of the disease, and that dyn-actin binds to microtubules and thus thatmutant dynactin may modify axonaltransport along microtubules. However,whether defective axonal transport is thecellular mechanism by which these

mutant proteins lead to motor neurondisease remains to be clearly established.Despite these uncertainties, demonstra-tion that mutations of each of these threegenes can cause familial ALS has givenscientists valuable clues about the molec-ular pathogenesis of at least some formsof this tragic disorder.

ReferencesADAMS, R. D. AND M. VICTOR (2001) Principlesof Neurology, 7th Ed. New York: McGraw-Hill, pp. 1152–1158.HADANO, S. AND 20 OTHERS (2001) A geneencoding a putative GTPase regulator ismutated in familial amyotrophic lateral scle-rosis 2. Nature Genetics 29: 166–173.PULS, I. AND 13 OTHERS (2003) Mutant dyn-actin in motor neuron disease. Nature Genet-ics 33: 455–456,ROSEN, D. R. AND 32 OTHERS (1993) Mutationsin Cu/Zn superoxide dismutase gene areassociated with familial amyotrophic lateralsclerosis. Nature 362: 59–62.YANG, Y. AND 16 OTHERS (2001) The geneencoding alsin, a protein with three guanine-nucleotide exchange factor domains, ismutated in a form of recessive amyotrophiclateral sclerosis. Nature Genetics 29: 160–165.

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gistic muscles. Gamma motor neurons regulate the gain of the stretch reflexby adjusting the level of tension in the intrafusal muscle fibers of the musclespindle. This mechanism sets the baseline level of activity in α motor neu-rons and helps to regulate muscle length and tone. Other reflex circuits pro-vide feedback control of muscle tension and mediate essential functionssuch as the rapid withdrawal of limbs from painful stimuli. Much of the spa-tial coordination and timing of muscle activation required for complexrhythmic movements such as locomotion are provided by specialized localcircuits called central pattern generators. Because of their essential role in allof these circuits, damage to lower motor neurons leads to paralysis of theassociated muscle and to other changes, including the loss of reflex activity,the loss of muscle tone, and eventually muscle atrophy.

Additional ReadingReviewsBURKE, R. E. (1981) Motor units: Anatomy,physiology and functional organization. InHandbook of Physiology, V. B. Brooks (ed.). Sec-tion 1: The Nervous System. Volume 1, Part 1.Bethesda, MD: American Physiological Soci-ety, pp. 345–422.BURKE, R. E. (1990) Spinal cord: Ventral horn.In The Synaptic Organization of the Brain, 3rdEd. G. M. Shepherd (ed.). New York: OxfordUniversity Press, pp. 88–132.GRILLNER, S. AND P. WALLEN (1985) Centralpattern generators for locomotion, with spe-cial reference to vertebrates. Annu. Rev. Neu-rosci. 8: 233–261.HENNEMAN, E. (1990) Comments on the logi-cal basis of muscle control. In The SegmentalMotor System, M. C. Binder and L. M. Mendell(eds.). New York: Oxford University Press, pp.7–10.HENNEMAN, E. AND L. M. MENDELL (1981)Functional organization of the motoneuronpool and its inputs. In Handbook of Physiology,V. B. Brooks (ed.). Section 1: The Nervous Sys-tem. Volume 1, Part 1. Bethesda, MD: Ameri-can Physiological Society, pp. 423–507.LUNDBERG, A. (1975) Control of spinal mecha-nisms from the brain. In The Nervous System,Volume 1: The Basic Neurosciences. D. B. Tower(ed.). New York: Raven Press, pp. 253–265.

PATTON, H. D. (1965) Reflex regulation ofmovement and posture. In Physiology and Bio-physics, 19th Ed., T. C. Rugh and H. D. Patton(eds.). Philadelphia: Saunders, pp. 181–206.PEARSON, K. (1976) The control of walking. Sci.Amer. 235 (Dec.): 72–86.PROCHAZKA, A., M. HULLIGER, P. TREND AND N.DURMULLER (1988) Dynamic and static fusimo-tor set in various behavioral contexts. InMechanoreceptors: Development, Structure, andFunction. P. Hnik, T. Soulup, R. Vejsada and J.Zelena (eds.). New York: Plenum, pp. 417–430.SCHMIDT, R. F. (1983) Motor systems. In HumanPhysiology. R. F. Schmidt and G. Thews (eds.).Berlin: Springer Verlag, pp. 81–110.

Important Original PapersBURKE, R. E., D. N. LEVINE, M. SALCMAN AND P.TSAIRES (1974) Motor units in cat soleus mus-cle: Physiological, histochemical, and mor-phological characteristics. J. Physiol. (Lond.)238: 503–514.BURKE, R. E., P. L. STRICK, K. KANDA, C. C. KIMAND B. WALMSLEY (1977) Anatomy of medialgastrocnemius and soleus motor nuclei in catspinal cord. J. Neurophysiol. 40: 667–680.HENNEMAN, E., E. SOMJEN, AND D. O. CARPEN-TER (1965) Excitability and inhibitability ofmotoneurons of different sizes. J. Neurophys-iol. 28: 599–620.

HUNT, C. C. AND S. W. KUFFLER (1951) Stretchreceptor discharges during muscle contrac-tion. J. Physiol. (Lond.) 113: 298–315.LIDDELL, E. G. T. AND C. S. SHERRINGTON (1925)Recruitment and some other factors of reflexinhibition. Proc. R. Soc. London 97: 488–518.LLOYD, D. P. C. (1946) Integrative pattern ofexcitation and inhibition in two-neuron reflexarcs. J. Neurophysiol. 9: 439–444.MONSTER, A. W. AND H. CHAN (1977) Isometricforce production by motor units of extensordigitorum communis muscle in man. J. Neu-rophysiol. 40: 1432–1443.WALMSLEY, B., J. A. HODGSON AND R. E. BURKE(1978) Forces produced by medial gastrocne-mius and soleus muscles during locomotionin freely moving cats. J. Neurophysiol. 41:1203–1215.

BooksBRODAL, A. (1981) Neurological Anatomy inRelation to Clinical Medicine, 3rd Ed. NewYork: Oxford University Press.SHERRINGTON, C. (1947) The Integrative Actionof the Nervous System, 2nd Ed. New Haven:Yale University Press.

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Overview

Eye movements are, in many ways, easier to study than movements of otherparts of the body. This fact arises from the relative simplicity of muscleactions on the eyeball. There are only six extraocular muscles, each of whichhas a specific role in adjusting eye position. Moreover, there are only fourstereotyped kinds of eye movements, each with its own control circuitry. Eyemovements have therefore been a useful model for understanding the mech-anisms of motor control. Indeed, much of what is known about the regula-tion of movements by the cerebellum, basal ganglia, and vestibular systemhas come from the study of eye movements (see Chapters 13, 17, and 18).Here the major features of eye movement control are used to illustrate theprinciples of sensory motor integration that also apply to more complexmotor behaviors.

What Eye Movements Accomplish

Eye movements are important in humans because high visual acuity isrestricted to the fovea, the small circular region (about 1.5 mm in diameter)in the central retina that is densely packed with cone photoreceptors (seeChapter 10). Eye movements can direct the fovea to new objects of interest (aprocess called “foveation”) or compensate for disturbances that cause thefovea to be displaced from a target already being attended to.

As demonstrated several decades ago by the Russian physiologist AlfredYarbus, eye movements reveal a good deal about the strategies used toinspect a scene. Yarbus used contact lenses with small mirrors on them (seeBox A) to document (by the position of a reflected beam) the pattern of eyemovements made while subjects examined a variety of objects and scenes.Figure 19.1 shows the direction of a subject’s gaze while viewing a picture ofQueen Nefertiti. The thin, straight lines represent the quick, ballistic eyemovements (saccades) used to align the foveas with particular parts of thescene; the denser spots along these lines represent points of fixation wherethe observer paused for a variable period to take in visual information (littleor no visual perception occurs during a saccade, which occupies only a fewtens of milliseconds). The results obtained by Yarbus, and subsequentlymany others, showed that vision is an active process in which eye move-ments typically shift the view several times each second to selected parts ofthe scene to examine especially interesting features. The spatial distributionof the fixation points indicates that much more time is spent scrutinizingNefertiti’s eye, nose, mouth, and ear than examining the middle of her cheekor neck. Thus, eye movements allow us to scan the visual field, pausing tofocus attention on the portions of the scene that convey the most significant

Chapter 19

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Eye Movementsand SensoryMotor Integration

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information. As is apparent in Figure 19.1, tracking eye movements can beused to determine what aspects of a scene are particularly arresting. Adver-tisers now use modern versions of Yarbus’ method to determine which pic-tures and scene arrangements will best sell their product.

The importance of eye movements for visual perception has also beendemonstrated by experiments in which a visual image is stabilized on theretina, either by paralyzing the extraocular eye muscles or by moving ascene in exact register with eye movements so that the different features ofthe image always fall on exactly the same parts of the retina (Box A). Stabi-lized visual images rapidly disappear, for reasons that remain poorly under-stood. Nonetheless, these observations on motionless images make it plainthat eye movements are also essential for normal visual perception.

The Actions and Innervation of Extraocular Muscles

Three antagonistic pairs of muscles control eye movements: the lateral andmedial rectus muscles, the superior and inferior rectus muscles, and thesuperior and inferior oblique muscles. These muscles are responsible formovements of the eye along three different axes: horizontal, either toward thenose (adduction) or away from the nose (abduction); vertical, either elevationor depression; and torsional, movements that bring the top of the eye towardthe nose (intorsion) or away from the nose (extorsion). Horizontal move-ments are controlled entirely by the medial and lateral rectus muscles; themedial rectus muscle is responsible for adduction, the lateral rectus musclefor abduction. Vertical movements require the coordinated action of thesuperior and inferior rectus muscles, as well as the oblique muscles. The rel-ative contribution of the rectus and oblique groups depends on the horizon-tal position of the eye (Figure 19.2). In the primary position (eyes straightahead), both of these groups contribute to vertical movements. Elevation isdue to the action of the superior rectus and inferior oblique muscles, whiledepression is due to the action of the inferior rectus and superior obliquemuscles. When the eye is abducted, the rectus muscles are the prime verticalmovers. Elevation is due to the action of the superior rectus, and depressionis due to the action of the inferior rectus. When the eye is adducted, theoblique muscles are the prime vertical movers. Elevation is due to the actionof the inferior oblique muscle, while depression is due to the action of thesuperior oblique muscle. The oblique muscles are also primarily responsiblefor torsional movements.

The extraocular muscles are innervated by lower motor neurons that formthree cranial nerves: the abducens, the trochlear, and the oculomotor (Figure19.3). The abducens nerve (cranial nerve VI) exits the brainstem from thepons–medullary junction and innervates the lateral rectus muscle. Thetrochlear nerve (cranial nerve IV) exits from the caudal portion of the mid-brain and supplies the superior oblique muscle. In distinction to all othercranial nerves, the trochlear nerve exits from the dorsal surface of the brain-stem and crosses the midline to innervate the superior oblique muscle on thecontralateral side. The oculomotor nerve (cranial nerve III), which exits fromthe rostral midbrain near the cerebral peduncle, supplies all the rest of theextraocular muscles. Although the oculomotor nerve governs several differ-ent muscles, each receives its innervation from a separate group of lowermotor neurons within the third nerve nucleus.

In addition to supplying the extraocular muscles, a distinct cell groupwithin the oculomotor nucleus innervates the levator muscles of the eyelid;the axons from these neurons also travel in the third nerve. Finally, the third

Figure 19.1 The eye movements of asubject viewing a picture of QueenNefertiti. The bust at the top is what thesubject saw; the diagram on the bottomshows the subject’s eye movements overa 2–minute viewing period. (FromYarbus, 1967.)

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Figure 19.3 Organization of the cra-nial nerve nuclei that govern eye move-ments, showing their innervation of theextraocular muscles. The abducensnucleus innervates the lateral rectusmuscle; the trochlear nucleus innervatesthe superior oblique muscle; and theoculomotor nucleus innervates all therest of the extraocular muscles (themedial rectus, inferior rectus, superiorrectus, and inferior oblique).

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Figure 19.2 The contributions of thesix extraocular muscles to vertical andhorizontal eye movements. Horizontalmovements are mediated by the medialand lateral rectus muscles, while verti-cal movements are mediated by thesuperior and inferior rectus and thesuperior and inferior oblique musclegroups.

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Box AThe Perception of Stabilized Retinal ImagesVisual perception depends critically onfrequent changes of scene. Normally, ourview of the world is changed by sac-cades, and tiny saccades that continue tomove the eyes abruptly over a fraction ofa degree of visual arc occur even whenthe observer stares intently at an object ofinterest. Moreover, continual drift of theeyes during fixation progressively shiftsthe image onto a nearby but different setof photoreceptors. As a consequence ofthese several sorts of eye movements(Figure A), our point of view changesmore or less continually.

The importance of a continuallychanging scene for normal vision is dra-matically revealed when the retinalimage is stabilized. If a small mirror is

attached to the eye by means of a contactlens and an image reflected off the mir-ror onto a screen, then the subject neces-sarily sees the same thing, whatever theposition of the eye: Every time the eyemoves, the projected image movesexactly the same amount (Figure B).Under these circumstances, the stabilizedimage actually disappears from percep-tion within a few seconds!

A simple way to demonstrate therapid disappearance of a stabilized reti-nal image is to visualize one’s own reti-nal blood vessels. The blood vessels,which lie in front of the photoreceptorlayer, cast a shadow on the underlyingreceptors. Although normally invisible,the vascular shadows can be seen bymoving a source of light across the eye, aphenomenon first noted by J. E. Purkinjemore than 150 years ago. This perceptioncan be elicited with an ordinary penlightpressed gently against the lateral side ofthe closed eyelid. When the light is wig-gled vigorously, a rich network of blackblood vessel shadows appears against anorange background. (The vessels appearblack because they are shadows.) Bystarting and stopping the movement, it isreadily apparent that the image of the

blood vessel shadows disappears withina fraction of a second after the lightsource is stilled.

The conventional interpretation of therapid disappearance of stabilized imagesis retinal adaptation. In fact, the phenom-enon is at least partly of central origin.Stabilizing the retinal image in one eye,for example, diminishes perceptionthrough the other eye, an effect knownas interocular transfer. Although theexplanation of these remarkable effects isnot entirely clear, they emphasize thepoint that the visual system is designedto deal with novelty.

ReferencesBARLOW, H. B. (1963) Slippage of contactlenses and other artifacts in relation to fadingand regeneration of supposedly stable retinalimages. Q. J. Exp. Psychol. 15: 36–51.COPPOLA, D. AND D. PURVES (1996) The ex-traordinarily rapid disappearance of entopicimages. Proc. Natl. Acad. Sci. USA 96:8001–8003.HECKENMUELLER, E. G. (1965) Stabilization ofthe retinal image: A review of method, effectsand theory. Psychol. Bull. 63: 157–169.KRAUSKOPF, J. AND L. A. RIGGS (1959) Interocu-lar transfer in the disappearance of stabilizedimages. Amer. J. Psychol. 72: 248–252.

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(B) Diagram illustrating one means of producing sta-bilized retinal images. By attaching a small mirror tothe eye, the scene projected onto the screen willalways fall on the same set of retinal points, no mat-ter how the eye is moved.

A) Diagram of the types of eye movementsthat continually change the retinal stimulusduring fixation. The straight lines indicatemicrosaccades and the curved lines drift; thestructures in the background are photo-receptors drawn approximately to scale. Thenormal scanning movements of the eyes(saccades) are much too large to be shownhere, but obviously contribute to the changesof view that we continually experience, asdo slow tracking eye movements (althoughthe fovea tracks a particular object, the scenenonetheless changes). (After Pritchard, 1961.)

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Figure 19.4 The metrics of a saccadiceye movement. The red line indicatesthe position of a fixation target and theblue line the position of the fovea. Whenthe target moves suddenly to the right,there is a delay of about 200 ms beforethe eye begins to move to the new targetposition. (After Fuchs, 1967.)

nerve carries axons that are responsible for pupillary constriction (see Chap-ter 11) from the nearby Edinger-Westphal nucleus. Thus, damage to the thirdnerve results in three characteristic deficits: impairment of eye movements,drooping of the eyelid (ptosis), and pupillary dilation.

Types of Eye Movements and Their Functions

There are four basic types of eye movements: saccades, smooth pursuitmovements, vergence movements, and vestibulo-ocular movements. Thefunctions of each type of eye movement are introduced here; in subsequentsections, the neural circuitry responsible for three of these types of move-ments is presented in more detail (see Chapters 13 and 18 for further discus-sion of neural circuitry underlying vestibulo-ocular movements).

Saccades are rapid, ballistic movements of the eyes that abruptly changethe point of fixation. They range in amplitude from the small movementsmade while reading, for example, to the much larger movements madewhile gazing around a room. Saccades can be elicited voluntarily, but occurreflexively whenever the eyes are open, even when fixated on a target (seeBox A). The rapid eye movements that occur during an important phase ofsleep (see Chapter 27) are also saccades. The time course of a saccadic eyemovement is shown in Figure 19.4. After the onset of a target for a saccade(in this example, the stimulus was the movement of an already fixated tar-get), it takes about 200 milliseconds for eye movement to begin. During thisdelay, the position of the target with respect to the fovea is computed (that is,how far the eye has to move), and the difference between the initial andintended position, or “motor error” (see Chapter 18), is converted into amotor command that activates the extraocular muscles to move the eyes thecorrect distance in the appropriate direction. Saccadic eye movements aresaid to be ballistic because the saccade-generating system cannot respond tosubsequent changes in the position of the target during the course of the eyemovement. If the target moves again during this time (which is on the orderof 15–100 ms), the saccade will miss the target, and a second saccade mustbe made to correct the error.

Smooth pursuit movements are much slower tracking movements of theeyes designed to keep a moving stimulus on the fovea. Such movements areunder voluntary control in the sense that the observer can choose whether ornot to track a moving stimulus (Figure 19.5). (Saccades can also be voluntary,but are also made unconsciously.) Surprisingly, however, only highly trainedobservers can make a smooth pursuit movement in the absence of a movingtarget. Most people who try to move their eyes in a smooth fashion withouta moving target simply make a saccade.

The smooth pursuit system can be tested by placing a subject inside arotating cylinder with vertical stripes. (In practice, the subject is more oftenseated in front of a screen on which a series of horizontally moving verticalbars is presented to conduct this “optokinetic test.”) The eyes automaticallyfollow a stripe until they reach the end of their excursion. There is then aquick saccade in the direction opposite to the movement, followed onceagain by smooth pursuit of a stripe. This alternating slow and fast move-ment of the eyes in response to such stimuli is called optokinetic nystag-mus. Optokinetic nystagmus is a normal reflexive response of the eyes inresponse to large-scale movements of the visual scene and should not beconfused with the pathological nystagmus that can result from certain kindsof brain injury (for example, damage to the vestibular system or the cerebel-lum; see Chapters 13 and 18).

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Figure 19.5 The metrics of smoothpursuit eye movements. These tracesshow eye movements (blue lines) track-ing a stimulus moving at three differentvelocities (red lines). After a quick sac-cade to capture the target, the eye move-ment attains a velocity that matches thevelocity of the target. (After Fuchs,1967.)

Vergence movements align the fovea of each eye with targets located atdifferent distances from the observer. Unlike other types of eye movementsin which the two eyes move in the same direction (conjugate eye move-ments), vergence movements are disconjugate (or disjunctive); they involveeither a convergence or divergence of the lines of sight of each eye to see anobject that is nearer or farther away. Convergence is one of the three reflex-ive visual responses elicited by interest in a near object. The other compo-nents of the so-called near reflex triad are accommodation of the lens, whichbrings the object into focus, and pupillary constriction, which increases thedepth of field and sharpens the image on the retina (see Chapter 10).

Vestibulo-ocular movements stabilize the eyes relative to the externalworld, thus compensating for head movements. These reflex responses pre-vent visual images from “slipping” on the surface of the retina as head posi-tion varies. The action of vestibulo-ocular movements can be appreciated byfixating an object and moving the head from side to side; the eyes automati-cally compensate for the head movement by moving the same distance butin the opposite direction, thus keeping the image of the object at more or lessthe same place on the retina. The vestibular system detects brief, transientchanges in head position and produces rapid corrective eye movements (seeChapter 13). Sensory information from the semicircular canals directs theeyes to move in a direction opposite to the head movement.

Although the vestibular system operates effectively to counteract rapidmovements of the head, it is relatively insensitive to slow movements or topersistent rotation of the head. For example, if the vestibulo-ocular reflex istested with continuous rotation and without visual cues about the move-ment of the image (i.e.,with eyes closed or in the dark), the compensatoryeye movements cease after only about 30 seconds of rotation. However, if thesame test is performed with visual cues, eye movements persist. The com-pensatory eye movements in this case are due to the activation of the smoothpursuit system, which relies not on vestibular information but on visual cuesindicating motion of the visual field.

Neural Control of Saccadic Eye Movements

The problem of moving the eyes to fixate a new target in space (or indeedany other movement) entails two separate issues: controlling the amplitude of

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movement (how far), and controlling the direction of the movement (whichway). The amplitude of a saccadic eye movement is encoded by the durationof neuronal activity in the lower motor neurons of the oculomotor nuclei. Asshown in Figure 19.6, for instance, neurons in the abducens nucleus fire aburst of action potentials prior to abducting the eye (by causing the lateralrectus muscle to contract) and are silent when the eye is adducted. Theamplitude of the movement is correlated with the duration of the burst ofaction potentials in the abducens neuron. With each saccade, the abducensneurons reach a new baseline level of discharge that is correlated with theposition of the eye in the orbit. The steady baseline level of firing holds theeye in its new position.

The direction of the movement is determined by which eye muscles areactivated. Although in principle any given direction of movement could bespecified by independently adjusting the activity of individual eye muscles,the complexity of the task would be overwhelming. Instead, the direction ofeye movement is controlled by the local circuit neurons in two gaze centersin the reticular formation, each of which is responsible for generating move-ments along a particular axis. The paramedian pontine reticular formation(PPRF) or horizontal gaze center is a collection of local circuit neurons nearthe midline in the pons responsible for generating horizontal eye move-ments (Figure 19.7). The rostral interstitial nucleus or vertical gaze center islocated in the rostral part of the midbrain reticular formation and is respon-sible for vertical movements. Activation of each gaze center separatelyresults in movements of the eyes along a single axis, either horizontal or ver-tical. Activation of the gaze centers in concert results in oblique movementswhose trajectories are specified by the relative contribution of each center.

An example of how the PPRF works with the abducens and oculomotornuclei to generate a horizontal saccade to the right is shown in Figure 19.7.Neurons in the PPRF innervate cells in the abducens nucleus on the sameside of the brain. There are, however, two types of neurons in the abducensnucleus. One type is a lower motor neuron that innervates the lateral rectus


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Figure 19.6 Motor neuron activity in relation to saccadic eyemovements. The experimental setup is shown on the right. In thisexample, an abducens lower motor neuron fires a burst of activity(upper trace) that precedes and extends throughout the movement(solid line). An increase in the tonic level of firing is associated withmore lateral displacement of the eye. Note also the decline in firingrate during a saccade in the opposite direction. (After Fuchs andLuschei, 1970.)

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Figure 19.7 Simplified diagram of syn-aptic circuitry responsible for horizontalmovements of the eyes to the right. Acti-vation of local circuit neurons in theright horizontal gaze center (the PPRF;orange) leads to increased activity oflower motor neurons (red and green)and internuclear neurons (blue) in theright abducens nucleus. The lowermotor neurons innervate the lateral rec-tus muscle of the right eye. The inter-nuclear neurons innervate lower motorneurons in the contralateral oculomotornucleus, which in turn innervate themedial rectus muscle of the left eye.

muscle on the same side. The other type, called internuclear neurons, sendtheir axons across the midline and ascend in a fiber tract called the mediallongitudinal fasciculus, terminating in the portion of the oculomotornucleus that contains lower motor neurons innervating the medial rectusmuscle. As a result of this arrangement, activation of PPRF neurons on theright side of the brainstem causes horizontal movements of both eyes to theright; the converse is of course true for the PPRF neurons in the left half ofthe brainstem.

Neurons in the PPRF also send axons to the medullary reticular forma-tion, where they contact inhibitory local circuit neurons. These local circuitneurons, in turn, project to the contralateral abducens nucleus, where theyterminate on lower motor neurons and internuclear neurons. In conse-quence, activation of neurons in the PPRF on the right results in a reductionin the activity of the lower motor neurons whose muscles would opposemovements of the eyes to the right. This inhibition of antagonists resemblesthe strategy used by local circuit neurons in the spinal cord to control limbmuscle antagonists (see Chapter 15).

Although saccades can occur in complete darkness, they are often elicitedwhen something attracts attention and the observer directs the foveastoward the stimulus. How then is sensory information about the location ofa target in space transformed into an appropriate pattern of activity in thehorizontal and vertical gaze centers? Two structures that project to the gazecenters are demonstrably important for the initiation and accurate targetingof saccadic eye movements: the superior colliculus of the midbrain, and aregion of the frontal lobe that lies just rostral to premotor cortex, known as

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the frontal eye field (Brodmann’s area 8). Upper motor neurons in both ofthese structures, each of which contains a topographical motor map, dis-charge immediately prior to saccades. Thus, activation of a particular site inthe superior colliculus or in the frontal eye field produces saccadic eyemovements in a specified direction and for a specified distance that is inde-pendent of the initial position of the eyes in the orbit. The direction and dis-tance are always the same for a given stimulation site, changing systemati-cally when different sites are activated.

Both the superior colliculus and the frontal eye field also contain cells thatrespond to visual stimuli; however, the relation between the sensory andmotor responses of individual cells is better understood for the superior col-liculus. An orderly map of visual space is established by the termination ofretinal axons within the superior colliculus (see Chapter 11), and this sensorymap is in register with the motor map that generates eye movements. Thus,neurons in a particular region of the superior colliculus are activated by thepresentation of visual stimuli in a limited region of visual space. This activa-tion leads to the generation of a saccade that moves the eye by an amountjust sufficient to align the foveas with the region of visual space that pro-vided the stimulation (Figure 19.8).

Neurons in the superior colliculus also respond to auditory and somaticstimuli. Indeed, the location in space for these other modalities also ismapped in register with the motor map in the colliculus. Topographicallyorganized maps of auditory space and of the body surface in the superiorcolliculus can therefore orient the eyes (and the head) in response to a vari-ety of different sensory stimuli. This registration of the sensory and motormaps in the colliculus illustrates an important principle of topographicalmaps in the motor system, namely to provide an efficient mechanism forsensory motor transformations (Box B).


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Figure 19.8 Evidence for sensory motor transformation obtained from electricalrecording and stimulation in the superior colliculus. (A) Surface views of the supe-rior colliculus illustrating the location of eight separate electrode recording and stim-ulation sites. (B) Map of visual space showing the receptive field location of the sitesin (A) (white circles), and the amplitude and direction of the eye movements elicitedby stimulating these sites electrically (arrows). In each case, electrical stimulationresults in eye movements that align the fovea with a region of visual space that cor-responds to the visual receptive field of the site. (After Schiller and Stryker, 1972.)

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The functional relationship between the frontal eye field and the superiorcolliculus in controlling eye movements is similar to that between the motorcortex and the red nucleus in the control of limb movements (see Chapter16). The frontal eye field projects to the superior colliculus, and the superiorcolliculus projects to the PPRF on the contralateral side (Figure 19.9). (It alsoprojects to the vertical gaze center, but for simplicity the discussion here is

Box BSensory Motor Integration in the Superior ColliculusThe superior colliculus is a laminatedstructure in which the differencesbetween the layers provide clues abouthow sensory and motor maps interact toproduce appropriate movements. Asdiscussed in the text, the superficial or“visual” layer of the colliculus receivesinput from retinal axons that form atopographic map. Thus, each site in thesuperficial layer is activated maximallyby the presence of a stimulus at a partic-ular point of visual space. In contrast,neurons in the deeper or “motor” layersgenerate bursts of action potentials thatcommand saccades, effectively generat-ing a motor map; thus, activation of dif-ferent sites generates saccades havingdifferent vectors. The visual and motormaps are in register, so that visual cellsresponding to a stimulus in a specificregion of visual space are locateddirectly above the motor cells that com-mand eye movements toward that sameregion (see Figure 19.8).

The registration of the visual andmotor maps suggests a simple strategyfor how the eyes might be guidedtoward an object of interest in the visualfield. When an object appears at a par-ticular location in the visual field, it willactivate neurons in the correspondingpart of the visual map. As a result,bursts of action potentials are generatedby the subjacent motor cells to com-mand a saccade that rotates the twoeyes just the right amount to direct thefoveas toward that same location in the

visual field. This behavior is called“visual grasp” because successful sen-sory motor integration results in theaccurate foveation of a visual target.

This seemingly simple model, for-mulated in the early 1970s when the col-licular maps were first found, assumespoint to point connections between thevisual and motor maps. In practice,however, these connections have beendifficult to demonstrate. Neither theanatomical nor the physiological meth-ods available at the time were suffi-ciently precise to establish these postu-lated synaptic connections. At about thesame time, motor neurons were foundto command saccades to nonvisualstimuli; moreover, spontaneous sac-cades occur in the dark. Thus, it wasclear that visual layer activity is notalways necessary for saccades. To con-fuse matters further, animals could betrained not to make a saccade when anobject appeared in the visual field,showing that the activation of visualneurons is sometimes insufficient tocommand saccades. The fact that activ-ity of neurons in the visual map is nei-ther necessary nor sufficient for elicitingsaccades led investigators away fromthe simple model of direct connectionsbetween corresponding regions of thetwo maps, toward models that linkedthe layers indirectly through pathwaysthat detoured through the cortex.

Eventually, however, new and bettermethods resolved this uncertainty.

Techniques for filling single cells withaxonal tracers showed an overlap be-tween descending visual layer axonsand ascending motor layer dendrites, inaccord with direct anatomical connec-tions between corresponding regions ofthe maps. At the same time, in vitrowhole-cell patch clamp recording (seeBox A in Chapter 4) permitted more dis-criminating functional studies that dis-tinguished excitatory and inhibitoryinputs to the motor cells. These experi-ments showed that the visual andmotor layers do indeed have the func-tional connections required to initiatethe command for a visually guided sac-cadic eye movement. A single brief elec-trical stimulus delivered to the superfi-cial layer generates a prolonged burst ofaction potentials that resembles thecommand bursts that normally occurjust before a saccade (see figure).

These direct connections presumablyprovide the substrate for the very shortlatency reflex-like “express saccades”that are unaffected by destruction of thefrontal eye fields. Other visual and non-visual inputs to the deep layers proba-bly explain why activation of the retinais neither necessary nor sufficient forthe production of saccades.

ReferencesLEE, P. H., M. C. HELMS, G. J. AUGUSTINE AND

W. C. HALL (1997) Role of intrinsic synapticcircuitry in collicular sensorimotor integra-tion. Proc. Natl. Acad. Sci. USA 94:13299–13304.

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limited to the PPRF.) The frontal eye field can thus control eye movementsby activating selected populations of superior colliculus neurons. This corti-cal area also projects directly to the contralateral PPRF; as a result, the frontaleye field can also control eye movements independently of the superior col-liculus. The parallel inputs to the PPRF from the frontal eye field and supe-rior colliculus are reflected in the deficits that result from damage to these


OZEN, G., G. J. AUGUSTINE AND W. C. HALL

(2000) Contribution of superficial layer neu-rons to premotor bursts in the superior col-liculus. J. Neurophysiol. 84: 460–471.SCHILLER, P. H. AND M. STRYKER (1972) Sin-gle-unit recording and stimulation in supe-rior colliculus of the alert rhesus monkey. J.Neurophysiol. 35: 915–924.SPARKS, D. L. AND J. S. NELSON (1987) Sen-sory and motor maps in the mammaliansuperior colliculus. TINS 10: 312–317.WURTZ, R. H. AND J. E. ALBANO (1980)Visual-motor function of the primate supe-rior colliculus. Annu. Rev. Neurosci. 3:189–226.

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(A) The superior colliculus receives visualinput from the retina and sends a commandsignal to the gaze centers to initiate a sac-cade (see text). In the experiment illustratedhere, a stimulating electrode activates cells inthe visual layer and a patch clamp pipetterecords the response evoked in a neuron inthe subjacent motor layer. The cells in thevisual and motor layers were subsequentlylabeled with a tracer called biocytin. Thisexperiment demonstrates that the terminalsof the visual neuron are located in the sameregion as the dendrites of the motor neuron.(B) The onset of a target in the visual field(top trace) is followed after a short intervalby a saccade to foveate the target (secondtrace). In the superior colliculus, the visualcell responds shortly after the onset of thetarget, while the motor cell responds later,just before the onset of the saccade. (C)Bursts of excitatory postsynaptic currents(EPSCs) recorded from a motor layer neuronin response to a brief (0.5 ms) current stimu-lus applied via a steel wire electrode in thevisual layer (top; see arrow). These synapticcurrents generate bursts of action potentialsin the same cell (bottom). (B after Wurtz andAlbano, 1980; C after Ozen et al., 2000.)

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Figure 19.9 The relationship of thefrontal eye field in the right cerebralhemisphere (Brodmann’s area 8) to thesuperior colliculus and the horizontalgaze center (PPRF). There are two routesby which the frontal eye field can influ-ence eye movements in humans: indi-rectly by projections to the superior col-liculus, which in turn projects to thecontralateral PPRF, and directly by pro-jections to the contralateral PPRF.

structures. Injury to the frontal eye field results in an inability to make sac-cades to the contralateral side and a deviation of the eyes to the side of thelesion. These effects are transient, however; in monkeys with experimentallyinduced lesions of this cortical region, recovery is virtually complete in twoto four weeks. Lesions of the superior colliculus change the accuracy, fre-quency, and velocity of saccades; yet saccades still occur, and the deficits alsoimprove with time. These results suggest that the frontal eye fields and thesuperior colliculus provide complementary pathways for the control of sac-cades. Moreover, one of these structures appears to be able to compensate (atleast partially) for the loss of the other. In support of this interpretation, com-bined lesions of the frontal eye field and the superior colliculus produce adramatic and permanent loss in the ability to make saccadic eye movements.

These observations do not, however, imply that the frontal eye fields andthe superior colliculus have the same functions. Superior colliculus lesions

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produce a permanent deficit in the ability to perform very short latencyreflex-like eye movements called “express saccades.” The express saccadesare evidently mediated by direct pathways to the superior colliculus fromthe retina or visual cortex that can access the upper motor neurons in thecolliculus without extensive, and more time-consuming, processing in thefrontal cortex (see Box B). In contrast, frontal eye field lesions produce per-manent deficits in the ability to make saccades that are not guided by anexternal target. For example, patients (or monkeys) with a lesion in thefrontal eye fields cannot voluntarily direct their eyes away from a stimulus inthe visual field, a type of eye movement called an “antisaccade.” Suchlesions also eliminate the ability to make a saccade to the remembered loca-tion of a target that is no longer visible.

Finally, the frontal eye fields are essential for systematically scanning thevisual field to locate an object of interest within an array of distractingobjects (see Figure 19.1). Figure 19.10 shows the responses of a frontal eyefield neuron during a visual task in which a monkey was required to foveatea target located within an arrray of distracting objects. This frontal eye field


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Figure 19.10 Responses of neurons inthe frontal eye fields. (A) Locus of theleft frontal eye field on a lateral view ofthe rhesus monkey brain. (B) Activationof a frontal eye field neuron duringvisual search for a target. The verticaltickmarks represent action potentials,and each row of tick marks is a differenttrial. The graphs below show the aver-age frequency of action potentials as afunction of time. The change in colorfrom green to purple in each row indi-cates the time of onset of a saccadetoward the target. In the left trace (1),the target (red square) is in the part ofthe visual field “seen” by the neuron,and the response to the target is similarto the response that would be generatedby the neuron even if no distractors(green squares) were present (notshown). In the right trace (3), the targetis far from the response field of the neu-ron. The neuron responds to the distrac-tor in its response field. However, itresponds at a lower rate than it would toexactly the same stimulus if the squarewere not a distractor but a target for asaccade (left trace). In the middle trace(2), the response of the neuron to thedistractor has been sharply reduced bythe presence of the target in a neighbor-ing region of the visual field. (AfterSchall, 1995.)

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neuron discharges at different levels to the same stimulus, depending onwhether the stimulus is the target of the saccade or a “distractor,” and on thelocation of the distractor relative to the actual target. For example, the differ-ences between the middle and the left and right traces in Figure 19.10demonstrate that the response to the distractor is much reduced if it islocated close to the target in the visual field. Results such as these suggestthat lateral interactions within the frontal eye fields enhance the neuronalresponses to stimuli that will be selected as saccade targets, and that suchinteractions suppress the responses to uninteresting and potentially distract-ing stimuli. These sorts of interactions presumably reduce the occurrence ofunwanted saccades to distracting stimuli in the visual field.

Neural Control of Smooth Pursuit Movements

Smooth pursuit movements are also mediated by neurons in the PPRF, butare under the influence of motor control centers other than the superior col-liculus and frontal eye field. (The superior colliculus and frontal eye field areexclusively involved in the generation of saccades.) The exact route bywhich visual information reaches the PPRF to generate smooth pursuitmovements is not known (a pathway through the cerebellum has been sug-gested). It is clear, however, that neurons in the striate and extrastriate visualareas provide sensory information that is essential for the initiation andaccurate guidance of smooth pursuit movements. In monkeys, neurons inthe middle temporal area (which is largely concerned with the perception ofmoving stimuli and a target of the magnocellular stream; see Chapter 11)respond selectively to targets moving in a specific direction. Moreover, dam-age to this area disrupts smooth pursuit movements. In humans, damage ofcomparable areas in the parietal and occipital lobes also results in abnormal-ities of smooth pursuit movements. Unlike the effects of lesions to the frontaleye field and the superior colliculus, the deficits are in eye movements madetoward the side of the lesion. For example, a lesion of the left parieto-occipi-tal region is likely to result in an inability to track an object moving fromright to left.

Neural Control of Vergence Movements

When a person wishes to look from one object to another object that arelocated at different distances from the eyes, a saccade is made that shifts thedirection of gaze toward the new object, and the eyes either diverge or con-verge until the object falls on the fovea of each eye. The structures and path-ways responsible for mediating the vergence movements are not well under-stood, but appear to include several extrastriate areas in the occipital lobe(see Chapter 11). Information about the location of retinal activity is relayedthrough the two lateral geniculate nuclei to the cortex, where the informa-tion from the two eyes is integrated. The appropriate command to diverge orconverge the eyes, which is based largely on information from the two eyesabout the amount of binocular disparity (see Chapter 11), is then sent viaupper motor neurons from the occipital cortex to “vergence centers” in thebrainstem. One such center is a population of local circuit neurons located inthe midbrain near the oculomotor nucleus. These neurons generate a burstof action potentials. The onset of the burst is the command to generate a ver-gence movement, and the frequency of the burst determines its velocity.

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There is a division of labor within the vergence center, so that some neuronscommand convergence movements while others command divergencemovements. These neurons also coordinate vergence movements of the eyeswith accommodation of the lens and pupillary constriction to produce thenear reflex discussed in Chapter 10.

Summary

Despite their specialized function, the systems that control eye movementshave much in common with the motor systems that govern movements ofother parts of the body. Just as the spinal cord provides the basic circuitry forcoordinating the actions of muscles around a joint, the reticular formation ofthe pons and midbrain provides the basic circuitry that mediates movementsof the eyes. Descending projections from higher-order centers in the superiorcolliculus and the frontal eye field innervate the brainstem gaze centers, pro-viding a basis for integrating eye movements with a variety of sensory infor-mation that indicates the location of objects in space. The superior colliculusand the frontal eye field are organized in a parallel as well as a hierarchicalfashion, enabling one of these structures to compensate for the loss of theother. Eye movements, like other movements, are also under the control ofthe basal ganglia and cerebellum (see Chapters 17 and 18); this controlensures the proper initiation and successful execution of these relatively sim-ple motor behaviors, thus allowing observers to interact efficiently with theuniverse of things that can be seen.


Additional Reading

ReviewsFUCHS, A. F., C. R. S. KANEKO AND C. A. SCUD-DER (1985) Brainstem control of eye move-ments. Annu. Rev. Neurosci. 8: 307–337.HIKOSAKA, O AND R. H. WURTZ (1989) Thebasal ganglia. In The Neurobiology of SaccadicEye Movements: Reviews of Oculomotor Research,Volume 3. R. H. Wurtz and M. E. Goldberg(eds.). Amsterdam: Elsevier, pp. 257–281.ROBINSON, D. A. (1981) Control of eye move-ments. In Handbook of Physiology, Section 1:The Nervous System, Volume II: Motor Control,Part 2. V. B. Brooks (ed.). Bethesda, MD:American Physiological Society, pp.1275–1319.SCHALL, J. D. (1995) Neural basis of targetselection. Reviews in the Neurosciences 6:63–85.

SPARKS, D. L. AND L. E. MAYS (1990) Signaltransformations required for the generation ofsaccadic eye movements. Annu. Rev. Neu-rosci. 13: 309–336. ZEE, D. S. AND L. M. OPTICAN (1985) Studies ofadaption in human oculomotor disorders. InAdaptive Mechanisms in Gaze Control: Facts andTheories. A Berthoz and G. Melvill Jones (eds.).Amsterdam: Elsevier, pp. 165–176.

Important Original PapersFUCHS, A. F. AND E. S. LUSCHEI (1970) Firingpatterns of abducens neurons of alert mon-keys in relationship to horizontal eye move-ments. J. Neurophysiol. 33: 382–392. OPTICAN, L. M. AND D. A. ROBINSON (1980)Cerebellar-dependent adaptive control of pri-mate saccadic system. J. Neurophysiol. 44:1058–1076.SCHILLER, P. H. AND M. STRYKER (1972) Singleunit recording and stimulation in superiorcolliculus of the alert rhesus monkey. J. Neu-rophysiol. 35: 915–924.

SCHILLER, P. H., S. D. TRUE AND J. L. CONWAY(1980) Deficits in eye movements followingfrontal eye-field and superior colliculus abla-tions. J. Neurophysiol. 44: 1175–1189.

BooksHALL, W. C. AND A. MOSCHOVAKIS (EDS.) (2004)The Superior Colliculus: New Approaches forStudying Sensorimotor Integration. Methodsand New Frontiers in Neuroscience Series.New York: CRC Press.LEIGH, R. J. AND D. S. ZEE (1983) The Neurologyof Eye Movements. Contemporary NeurologySeries. Philadelphia: Davis.SCHOR, C. M. AND K. J. CIUFFREDA (EDS.) (1983)Vergence Eye Movements: Basic and ClinicalAspects. Boston: Butterworth.YARBUS, A. L. (1967) Eye Movements and Vision.Basil Haigh (trans.). New York: Plenum Press.

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