Windhorst - Muscle proprioceptive feedback and spinal networks.pdf

Brain Research Bulletin 73 (2007) 155202

Review

Muscle proprioceptive feedback and spinal networksU. Windhorst

Abstract

This revieas spinal recgeneration oand correcticompensatiointeraction fof spinal cir 2007 Else

Keywords: Sp

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1572. Organization of scratch reflexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1573. Rhythmogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1594. Generation of upright body posture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

4.1. Generation of anti-gravity thrust and stiffness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160

4.2.4.3.

5. Musc5.1.

5.2.5.3.

Tel.: +49E-mail ad

0361-9230/$doi:10.1016/j4.1.1. Decerebrate rigidity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1604.1.2. Core stretch reflex circuit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160Reciprocal Ia inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162Recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1624.3.1. Prevalence of recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1634.3.2. Core recurrent inhibitory circuits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163

le proprioceptive feedback and recurrent inhibition in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164Muscle spindles and Golgi tendon organs in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.1. Golgi tendon organ discharge in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.2. Muscle spindle discharge in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.3. Follow-up length servo hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.4. Servo-assistance hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.5. - and -motoneuron discharge patterns in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1645.1.6. Supraspinal and sensory inputs to - and -motoneurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166Modulation of segmental sensory input by presynaptic inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166Reciprocal inhibition in action. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167

551 380405; fax: +49 551 3792135.dress: [email protected].

see front matter 2007 Elsevier Inc. All rights reserved..brainresbull.2007.03.010Center for Physiology and Pathophysiology, University of Goettingen, Humboldtallee 23, D-37073 Goettingen, GermanyReceived 15 March 2007; accepted 15 March 2007

Available online 17 April 2007

w revolves primarily around segmental feedback systems established by muscle spindle and Golgi tendon organ afferents, as wellurrent inhibition via Renshaw cells. These networks are considered as to their potential contributions to the following functions: (i)f anti-gravity thrust during quiet upright stance and the stance phase of locomotion; (ii) timing of locomotor phases; (iii) linearizationon for muscle nonlinearities; (iv) compensation for muscle lever-arm variations; (v) stabilization of inherently unstable systems; (vi)n for muscle fatigue; (vii) synergy formation; (viii) selection of appropriate responses to perturbations; (ix) correction for intersegmentalorces; (x) sensory-motor transformations; (xi) plasticity and motor learning. The scope will at times extend beyond the narrow confinescuits in order to integrate them into wider contexts and concepts.vier Inc. All rights reserved.

inal cord; Motoneurons; Muscle spindles; Golgi tendon organs; Recurrent inhibition

156 U. Windhorst / Brain Research Bulletin 73 (2007) 155202

5.4. Recurrent inhibition in action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1675.4.1. Recurrent inhibition in cat fictive locomotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1675.4.2. Recurrent inhibition of reciprocal inhibition in cat fictive locomotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

5.5.

5.6.5.7.

5.8.

6. Stabi6.1.6.2.

6.3.

7. Comp7.1.7.2.

8. Summ9. Glob

9.1.9.2.

9.3.9.4.

10. Post10.1.10.2.Compensation for muscle properties and joint nonlinearities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1685.5.1. Linearization of muscle stiffness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1685.5.2. Coping with muscle forcelengthvelocity relationships . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1685.5.3. Compensation for joint lever-arm variations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1685.5.4. In search of a role for Golgi tendon organs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169Spinal actions of group Ib afferents from Golgi tendon organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169Sensory force feedback during the stance phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1695.7.1. Contributions of sensory receptors to force feedback. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1695.7.2. Golgi tendon organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1705.7.3. Muscle spindle group Ia afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1705.7.4. Muscle spindle group II afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1705.7.5. Intermediate summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170Interactions between sensory feedback and pattern generators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1715.8.1. Stance-to-swing transition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1715.8.2. Drawing inferences and making choices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171

lization of motor output . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171Positive force feedback: risk of instability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171Motor output fluctuations, muscle proprioceptors and recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1726.2.1. Physiological tremor and muscle proprioceptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1726.2.2. Physiological tremor and recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1736.2.3. Intermittent motor control and muscle proprioceptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173Compensation for reflex delays . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1736.3.1. Compensation of muscle-unit dynamics by -motoneuron discharge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1736.3.2. Phase advance by muscle spindle dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1736.3.3. Phase advance by recurrent inhibition? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174

ensation for muscle fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174Actions of the stretch reflex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174Muscular wisdom . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1747.2.1. -Motoneuron discharge adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.2. Diminishing descending motor commands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.3. Diminishing support from neuromodulatory systems? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.4. Diminishing facilitation from muscle spindle afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.5. Actions of chemosensitive group IIIIV muscle afferents on spinal neurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.6. Actions of chemosensitive group IIIIV muscle afferents on -motoneurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1757.2.7. Actions of chemosensitive group IIIIV muscle afferent fibers on -motoneurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1767.2.8. Actions on Ib inhibitory interneurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1767.2.9. Actions on recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1767.2.10. Actions on interneurons mediating presynaptic inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176ary and comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177

al roles of proprioceptive afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177The redundancy problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178Global variables of limb geometry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1789.2.1. Cat quiet stance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1789.2.2. Cat and human locomotion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1789.2.3. Biomechanics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1789.2.4. Neural control mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179Synergies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179Involvement of muscle proprioceptors and recurrent inhibition in synergy formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1799.4.1. Coping with muscle complexity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1799.4.2. Coping with multiple degrees of freedom at a joint . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1809.4.3. Intermediate summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1809.4.4. Heteronymous connections of muscle spindle group Ia afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1819.4.5. Heterogenic connections of muscle spindle group II afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1819.4.6. Heterogenic connections of Golgi tendon organ afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1819.4.7. Heterogenic connections of recurrent inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1829.4.8. Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182

ural maintenance and adjustments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183Multiplicity of body schemata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184Postural body schema . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184

U. Windhorst / Brain Research Bulletin 73 (2007) 155202 157

10.3. Role of proprioceptors in human body sway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18410.3.1. The case against group Ia afferents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18410.3.2. Alternative sensory afferents involved in sway control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

10.4. Role of proprioceptors in human postural reactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18510.5. Automatic postural responses in cats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18510.6.

11. Prop11.1.11.2.11.3.11.4.

12. Plas12.1.12.2.12.3.12.4.

13. Tran13.1.13.2.13.3.

14. FinaConAckRefe

1. Introdu

Can seAlready twexperimentriches init is usefulThose whoto be well-centers oftex and certhe shiftinunpublisheshaw cell (icollateralsdiscoverer:simplicityflow, our faan embarasputationalwill yield uquest for uYes and no

As requaround segdle and Go

1 The termword propriuAnticipatory postural adjustments to self-generated movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186rioceptive feedback in intersegmental interaction dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186

Cat paw shake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186Cat walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187Human arm reaching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

ticity, adaptability and learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187Learning kinematics and dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187Restoration of function after spinal cord injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188Plasticity of the stance support system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188A hypothesis on the role of recurrent inhibition in learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189

12.4.1. Back-propagating action potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18912.4.2. Influence of inhibition on back-propagating action potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18912.4.3. Corollaries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19012.4.4. Operation of the model after neurectomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190

sformations revisited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190Spatial representations and transformations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190Coding of kinematics and kinetics in dorsal spinocerebellar tract cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191Kinematickinetic mixtures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

l comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193flict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193nowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193rences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

ction

nse be made of spinal interneuron circuits? [247].o decades ago, Loeb [214] wrote: Those whoses have forced us to confront the embarassment ofthe workings of the spinal cord must ask whetherto continue to collect yet more inexplicable data.believed the spinal cord and peripheral motor plant

understood and thus turned their attentions to highermotor planning and coordination (e.g. cerebral cor-ebellum) now find that their edifices are built upong sands of spinal segmental circuitry (Stuart, D.G.,d) (p. 111). Addressing the sense of the spinal Ren-ntercalated in the inhibitory circuit from motor axonto ventral horn neurons and named in honor of itsRenshaw [308]), Zev Rymer felt that, given the

of the circuit, and its direct proximity to motor out-ilure to clarify the function of the Renshaw neuron issment, and does not generate confidence that com-

approaches used to describe complex neural circuitsseful answers (cited in ref. [391], p. 520). Does ournderstanding spinal circuits end in embarassment?, as discussed below.ested by the editor, this review will revolve primarilymental feedback systems established by muscle spin-lgi tendon organ afferents (muscle proprioceptive1

proprioception is ambivalent because it is composed of the Latins (own) and a truncated second part, which could refer to recep-

afferents), as well as spinal recurrent inhibition via Renshawcells. At first glimpse, this association appears somewhat arbi-trary, but it has a long tradition. The discussion will thus focuson spinal circuits, but since segments neither in the spinal cordnor in the body and limbs are isolated, the view will at times haveto fly out beyond the narrow confines of spinal circuits in orderto integrate them into wider concepts. The literature on theseissues is immense, and the selection is necessarily restrictiveand subjective.

2. Organization of scratch reexes

In the 19th and first half of the 20th century, the spinal cordwas considered, besides as a conductive structure, primarily as areflex machine. The application of the term reflex to such actsseems to have been made first by Descartes (1649), on the anal-ogy of the reflection of light, the sensory effect in these cases

tion or perception. In this sense, proprioceptor is clearer by referring to theperipheral sensory receptors (proprio-receptor). Proprioceptors are classicallydefined as being activated by mechanical stimuli arising from the bodys self-generated motor actions [94,140,339]. Prochazka [299] subsumes under thisrubric all the receptors that carry signals related to these variables, irrespectiveof whether the signals reach consciousness or contribute to movement controlat subconscious levels. Proprioceptors comprise a fairly wide group of differ-ent mechano-receptors, from muscle receptors (muscle spindles, Golgi tendonorgans, arguably some mechanically excitable free nerve endings), joint andligament receptors, to cutaneous mechano-receptors, which can be excited bystimuli impinging on them from both the exterior and interior world, thus beingboth exteroceptors and proprioceptors.


being reflected back, so to speak, as a motor effect ([150], p.141). The optic analogy suggests a deceiving simplicity, whichillusion apapply in caing neuroloin case of[291,324].careful anasolve by mfeedback.

Consideing reflex. Wlegs fixed apiece of paright hindlremoving tare placedponent), thfollowed bclose to thein a rhythming phase.composedvarying extulus, and tSimilar featurtle [350]

A bit m[194]. Supstimulus odiagonallyflexion witweight is sThe scratchtions at a foften in aing positiodynamic mshakes, indnized in thexecute pawfrequencyis shorteneof organizigests that tpattern gencourse.

Overall,muscular istimulus anendpoint bthis motormultiple fe

Excitatiothe scratreceptor

movement onset (due to possible fusimotor effects on musclespindles) and when the movement is underway, propriocep-

chaneratribe

initiasted

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ffect

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peripuisitesclepears to have survived until today. Indeed, it mayse of the artificial tendon reflex used by hammer-gists to test the excitability of the spinal cord, and

the even more artificial, and most popular, H-reflexNatural reflexes can be complex, however, and theirlysis reveals problems, which the spinal cord has toeans that in many respects involve proprioceptive

r a seemingly simple behavior, namely the frogs wip-hen a spinalized frog is put on a platform with three

nd only the right hindleg free to move, and a smallper soaked with acid is put on the right forearm, theeg will perform a sequence of movements aimed athe noxious stimulus. First, the toes of the hindlegclose to the stimulus (positioning or postural com-en the paper is whisked away (extension movement),y another flexion movement bringing the toes backstimulus, and these latter two phases may be repeatedic fashion depending on the success of the first whisk-This complex movement pattern in space and time,of several distinct components, can be adapted toernal circumstances such as the position of the stim-he frogs body configuration [23,105,176,295,331].tures characterize the scratch reflex of the spinalized.

ore complicated is the cats or dogs scratch reflexpose, for example, a standing cat is irritated by an one pinna. The cat will lift an ipsilateral hindlegtoward the head by a combination of hip and ankle

h knee extension (approach), while part of the bodyhifted to the other legs, thus stabilizing the body.ing limb then falls into a sequence of 160 oscilla-requency of 48 Hz. Scratching is performed mostsitting posture and sometimes in a lying or stand-n, with different initial conditions for the followingotor act [194]. Even spinalized cats can perform pawicating that the basic underlying functions are orga-e spinal cord [317]. Furthermore, spinal cats can

shakes simultaneously with walking. Although theof stepping is reduced in this condition and stanced and swing prolonged, the spinal cord is capableng the two behaviors simultaneously [49]. This sug-he two behaviors are organized by different centralerators (see below), which must be coordinated, of

the motor task of the nervous system and its skeleto-nstruments consists of localizing the initializingd converting it into a kinematic trajectory of the limby generating the appropriate kinetics. Conceptually,act can be broken down into a series of events, withedback effects:

n of appropriate sensory receptors. Obviously, inch reflex (and similar reflexes), cutaneous sensorys are first excited to get the reflex going. Even before

tors Gen

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theexqa muge their discharge and influence the progress.ion of initial posture and postural adjustments. Asd above, the scratch reflex may start from differ-l postures that must be generated and appropriatelyfor the reflex as well as secured against external

nces (Section 10).genesis. The rhythmical component of the scratchng reflexes and other rhythmical movements dependal rhythm generators (Section 3).motor transformations. The entire motor act involvesransformations:ization. The localization of stimulus and goal mustresented within the central nervous system (CNS) inbodily reference frame, which is usually referred toody schema, in whose construction proprioceptorsn important part (Section 10).l transformations. Target-oriented movementse the determination of target location with respectmoving body part, in wiping and scratch reflexesll as in voluntary arm reaching. Different func-elements of the reflex-generating system work in

ent frames of reference, however. Thus, cutaneousors are arrayed in a two-dimensional sheet folded indimensional space; each fusiform muscle develops

essentially in an intrinsic one-dimensional direc-joint angles span an intrinsic one-dimensional todimensional space (depending on joint type: hingel-and-socket joint); endpoint movement occurs intrinsic three-dimensional space; and the elicitedoceptor activities are specified in an intrinsicimensional to three-dimensional space (dependingeptor type). These different representations requirel transformations between the frames of referenceon 13).atic-to-kinetic and kinetic-to-kinematic transforma-Sensory inputs are, at least to some extent, cast inatic terms related to movement, while muscle activ-chieve kinematic goals in terms of kinetic (dynamic)les related to forces. This requires kinematic-to-c transformations, generating the daunting inverseics problem [295] (Section 13). Conversely, thef muscle activations is a movement trajectory inal space, implying that muscle forces must be trans-d into muscle torques, these into (compound) joints (influenced by other torques such as gravitationalter-segment interaction torques; Section 11), theseint-angle changes, and these into a paw movementThis sequence of events (with inherent feedback

s) must be taken into account by the spinal cord.

-skeletal properties. Some problems the CNS has ing movements arise from the complex properties ofheral musculo-skeletal system. Muscle operation isly nonlinear, dependent on activation history and ons linkage to bones, which must be taken into account


by the CNS in organizing neural commands to muscles (Sec-tion 5.5).

Stabilization. Several inherent properties render the neuro-muscular system prone to various types of oscillatoryinstability, which must be controlled by the CNS (Section6).

Muscle fatigue is an inherent property of the neuro-muscularsystem, w7).

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activation patterns need to be tailored to the peripheralbiomechanics of the limb and the muscles acting on it. Con-ceptuaan intsystem

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alanrojecase ordin, truilizacanhich must be kept in check as far as possible (Section

int coordination. Posture and movement are executed-joint systems, which pose much more severe prob-n single-joint systems (Sections 911).ncy reduction. There is no unique mapping of joint-nfigurations onto end-point locations, which causesancy problem (Section 9).ility and plasticity. Neuro-muscular systems must bedapt to changing environments, requiring plasticitynal networks (Section 12).

t contains sub-functions, most of which have beeninvolve proprioceptive feedback in some way. The lists a guideline of the following discussion, which willgeneral view and transcend the particular paradigm

ng or scratch reflex, however.

ogenesis

r to produce the rhythmic scratch-reflex compo-ll as other rhythmic movements (e.g., locomotion,, respiration), the CNS makes use of complexf neurons, which are generally called central pat-tors (CPGs) [185]. While in principle they may

ythmic motoneuron activities without sensory feed-ignals descending from supraspinal structures, thesee the timing and magnitude of motoneuron activ-heir processing is conversely influenced by CPGs8,280,282,317,355]. The organization and operationill be mentioned only in passing.

c pattern generation. Conceptually, locomotor CPGsivided into [40,120,160,202,320,321]:m-generating networks (clocks). The first require-is the existence of a clock or clocks to provide forndamental frequency of the rhythm. As a matter ofhis frequency must be variable to accommodate thent gaits.n-formationnetworks shape excitatory and inhibitorynal waveforms and distribute them in various com-ons to the different skeleto-motoneuron2 pools so aserate coordinated muscle activation patterns. Thison-trivial task because the spatio-temporal muscle

otoneurons innervate the (extrafusal) large muscle fibers in skele-oing the main muscle work. In mammals, skeleto-motoneuronsto pure skeleto-motoneurons called -motoneurons, which do justotoneurons that innervate extra- and intrafusal muscle fibers ines. For simplicity, we will refer to both classes as -motoneurons.

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Stabturelly, therefore, the coordinating network incorporatesernal model of the peripheral musculo-mechanical.

ent and adaptation to prevailing circumstances. Theor activation patterns must be implemented in andto a complex and dynamically changing environment282,317]. The actual circumstances include externals, such as terrain, surface properties, obstacles, qual-he medium (air, water, ground, surface), additionalnd resistances (e.g., wind), and internal propertiesoving body, such as musculo-skeletal and nervouss and perturbations. The actual muscle activationmust therefore be properly adapted by sensory feed-luding muscle proprioceptive and cutaneous signals

317]. The importance of sensory feedback is indi-the fact that cat locomotion is more normal and stable,uable and more easily adjustable to a wider range ofith than without intact sensory feedback [129,299].

lies more generally to other motor activities includingy goal-directed and manipulative movements, whichseverely disturbed after de-afferentation [116] (Sec-). Moreover, when a swinging leg hits an obstacle on

dorsum, the movement should not be carried throught, but changed so as to allow the foot to circumvent the. This requires that cutaneous/proprioceptive signals

(reset, re-program) the locomotor CPG. Conversely,ficance of various sorts of sensory signals changesspecific task (stance, walking, running, etc.) and,ch task, with the phase of the cycle, during which thevironment relation is changing dynamically. Hence,xes and other motor activities based on sensory sig-ld also change in a way adapted to the instantaneous

ns. This requires that reflexes be plastic rather thanle. In fact, all known spinal reflex pathways areduring locomotion by way of various mechanisms

48,280,282,317,410].

tion of upright body posture

pright stance of animals suspending their body aboveby means of legs, the controlling neural system

t the following general requirements:

vity function [236]:ation of upward thrust by provision of muscle tonei-gravity muscles.ce. Under stationary conditions of upright stance, thetion of the bodys center of mass must fall within thef support.ation of proper muscle torques across the series ofnk and neck joints.tion of posture against de-stabilizing influences. Pos-be perturbed by acceleration forces resulting from:


Internal perturbations. Breathing, heart beat, neural noise,muscle tremor (Section 6.2), muscle fatigue (Section 7).

Moveforcesas an

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Sensory feedback and associated central control systems helpregulate limb biomechanics and stance. Reflex-mediated stiff-

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helpments of other body parts through inertial interaction. While standing, movements of body segments sucharm will change the distribution of body mass ass exert inertial interaction forces between the bodynts (Section 11). In order to preserve equilibrium,S must take these actions into account in advance,

ay precisely calibrated to movement direction andty (Section 10.6).al inuences, including gravity and interactions with

vironment (e.g., changes in support, sudden bus stops,s to the body, sudden obstacles).onandprediction of themultiple types of forces actingdy, including its own muscle forces, gravitation, iner-

actions between segments, friction between segmentseen body and environment, and their interactions

his requires the use, processing and integration ofr, proprioceptive and cutaneous afferent signals.representation of an appropriate posture in terms ofal body schema, including a representation of theonfiguration and its relationships with the externalection 10.2).

e a number of means for the body to solve the abovehe central role is occupied by the CNS, which mustand produce muscle forces so as to complement

nate all other forces acting on the body [146]. Theseepend significantly on proprioceptive feedback.

ation of anti-gravity thrust and stiffness

terrestrial animals and humans upright on their legsechanisms to resist external disturbances, includingis stiffness is provided by at least three mechanisms7,148,239]:

tions from skeleto-articular elements. For exam-umans and large quadrupeds such as elephants andupright stance is supported to a considerable extentnatomical alignment of limb segments, thus engag-ective tissues to provide the required stiffness whileing muscular forces [146].stic properties of passive muscles provide (small)and automatic compensation for load changes duringearing.ing muscle activity, which can be minimized, how-keleto-articular contributions. In smaller quadrupedsogs and cats, the hindlegs are fairly flexed, whereby

uscle forces are needed to maintain the relative exten-inst the flexing forces due to gravity [146]. Tonicontraction renders the muscle more resistant to exten-ording to its lengthtension characteristics. In cats,e of soleus muscle lengths during quiet standing andion covers the steep part of the lengthtension curve

ness

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Sheinterprunderlstretchis whit? Lithis . .

4.1.2.The

stretchcontacnism aAlthoutypesciplesmusclecircuit(that)ults from the actions of the stretch reflex (below),cruits additional -motoneurons and increases thee of already active -motoneurons. This feedback isy related to load or force and acts to enhance muscleactivity (Section 5.7).

t three mechanisms are the fast-acting first line ofoviding a load-compensation mechanism and thusstural sway and yield to gravity during quiet stance.iated stiffness may add to the first defence, but atepending on conduction, synaptic and contraction

nt of the active muscle work has to be carried by theal limb extensor (anti-gravity) muscles, which also provide for most of the stiffness. This is welly the phenomenon of decerebrate rigidity, which will

a heuristic primer.

erebrate rigidityated limb extensions occur under a variety of patho-umstances, particularly in decerebrate rigidity. In

he animal (usually cat or dog) extends its limbs, theil, to the extent that the activity in anti-gravity mus-

ng enough to enable upright stance (review of early123,239]).uch-simplified view, there are two experimentalproducing decerebrate rigidity. Anemic decerebra-produces extensor muscle activity predominantly

r-activity of -motoneurons, whereby it is classi-red to as -rigidity [123,239]. The second typears when the brainstem of a cat or dog is severedrcollicular level of the midbrain, and is character-dditional increase in -motoneuron activity, therebyma type of rigidity ([123], p. 165). Note that bothidity provide for both anti-gravity upward thrust and

tons [338] classical decerebrate posture has beenas reflex standing. Sherrington showed that themechanism is associated with exaggerated extensorxes. An immediate question about the stretch reflexf the various receptors in muscle is responsible for

l & Sherrington wisely refrained from comment on39], p. 421).

e stretch reex circuitplest possible reflex mechanism is based on musclesitive sensory receptors and their monosynapticith homonymous -motoneurons. Such a mecha-rs fundamental in being phylogenetically ancient.

arthropods, amphibia and mammals use differentoprioceptors, they use similar organizational prin-at proprioceptive organs lie in parallel to skeletalers and excite homonymous motoneurons. Thisbeen interpreted as a postural negative feedback

s to maintain a given position ([58], p. 199). The


stretch receptors in mammals differ significantly from thosein invertebrates, however.

In vertemonosynapdles [19,29tendon orgreceptors toappear in aonly one setic contactsspindle is ming and assIa afferent[19]. Theirdifferent st

In mamcould provinaptic con-motoneudevelopmetional anatoIn parallel,general, th-motoneuinnervatingrelationshipsynaptic pThus, thosing postur[38]), recei[361].

Group Imake a smexcitationIa actionspolysynaptOtherwise,reflex actiotions 5.7.4

SherringFirst, aftertract desceis enhanceto extensocle tone. S-motoneuwhose enhawhich in tuextensor mper se provThird, the sdisturbanceunder thedecrease oraise their d-motoneutraction to

Schematic diagram of the monosynaptic stretch reflex circuit for catb muscles. Each neural element represents a population. Excitatory neu-symbolized by open circles and their synapses by T junctions. At thea hindleg is sketched with outlines of the ankle flexor muscles (left) andtensor muscle (right). The muscles contain muscle spindles symbolizedht lines with coils (primary sensory endings) around their middle por-

pindles lie in parallel to the main skeletal muscle fibers. They receiveinnervation from -motoneurons and from branches of -motoneuronslled -motoneurons, see footnote 2). Group Ia afferents originate fromendings on muscle spindles and project to the spinal cord, in which

ke monosynaptic excitatory connections to -motoneurons of their ownymous) muscle and of synergistic muscles (Section 9.4.4). - and -rons receive a variety of excitatory and inhibitory inputs from segmentalpropriospinal and supraspinal sources, symbolized by the dashed arrows

) should therefore depend on an intact reflex loop, whichit does, since severance of the dorsal roots abolishes much

rigidity [239].rrington [340] summarized his view of reflex standing inbrate cats as follows: A peculiarity which distinguishesetch reflex from other reflexes is that . . . the stretch reflexin its limb just the one muscle stretched. The reflex stand-the limb is a harmonious congeries of stretch reflexes,omponent reflex being the self-operating reaction of anual extensor muscle (p. 929). This quotation contains

teresting ideas. First, stretch reflexes are here consideredices to stabilize muscle length in quiet stance. Second,brates, the stretch-sensitive muscle receptors withtic connections to motoneurons are the muscle spin-9]. (Among stretch-sensitive receptors are also Golgians and some non-muscular cutaneous mechano-be dealt with later.) Evolutionarily, muscle spindles

nurans (frogs and toads). In these, each spindle hasnsory ending whose afferent fiber makes monosynap-

with motoneurons [342]. The mammalian muscleore complicated in having two types of sensory end-ociated afferent: the primary ending with its group

and the secondary ending(s) with group II afferent(s)monosynaptic connections to -motoneurons are ofrength (below).mals, then, the simplest stretch-reflex circuit thatde for stretch-mediated stiffness consists of monosy-nections from group Ia afferents to homonymousrons, as illustrated in Fig. 1. (For the ontogeneticnt of this circuit, see ref. [51], and for a detailed func-my of Iamotoneuron connections, see ref. [220].)there exist oligosynaptic linkages (see below). In

e strongest monosynaptic Ia-connections exist withrons involved in postural tasks, particularly thoseanti-gravity muscles, and in these cases an inverseholds between monosynaptic Ia excitatory post-

otential size and the size of the -motoneurons.e motor units, which are predominantly active dur-al tasks (S-type units with small -motoneuronsve the strongest monosynaptic Ia afferent feedback

I afferents from secondary muscle spindle endingsaller monosynaptic contribution to -motoneuronand might thus support the monosynaptic group

[186,239,349]. Moreover, excitatory oligo- oric connections might contribute their share [239].group II afferents produce a bewildering variety ofns [164,329], which will be dealt with below (Sec-and 9.4.5).tons reflex standing could come about as follows.decerebration the activity of the vestibulospinal

nding from Deiters (lateral vestibular) nucleusd, thus generating an augmented excitatory driver -motoneurons and increasing extensor mus-econd, the vestibulospinal tract excites, besides

rons, the associated homonymous -motoneurons,nced activity provides excitatory bias to the spindles,rn reflexly excite -motoneurons and thus enhanceuscle activity indirectly. This enhanced static toneides for increased stiffness (resistance to change).trong stretch reflex action adds to resistance againsts. Thus, when an extensor muscle slightly yieldsimpact of body weight or an accidental internalf muscle tension, its muscle spindles are stretched,ischarge rate and reflexly excite their homonymous

rons, which thus increase anti-gravity muscle con-resist the yield. This gamma type of rigidity ([123],

Fig. 1.hindlimrons are

bottom,ankle exas straigtions. Sa motor(here caprimarythey ma(homonmotoneusensory,on top.

p. 165indeedof the

Shedecerethe strexcitesing ofeach cindividtwo inas dev


stretch reflexes appear as self-operating reactions of individualextensor muscles.

The imphas recentlthat are unpostures duafferents in

For unktions maymuscles. Fof dihydroreflexes in bstanding onstance, inactivation.circuits als

4.2. Recip

There acoordinatedextensor mwould stretstretch reflcould lead-motoneuinhibited sagonists.

Thus, astant spinalonto segme-motoneucerebellar t

ReciproWhen exteonist flexoIa afferentmous -m-motoneuand impaircan be preinterneuron(Fig. 2). Musome sub-p

4.3. Recur

The precthe evolutiwhose remof thinkingproblem infusimotor csized to loof fluctuatilimit the ex[178]. Wh

implified diagram of monosynaptic excitation and reciprocal inhibitionby muscle spindle group Ia afferents. Excitatory neurons are symbol-open circles and their synapses by T junctions. Inhibitory interneuronsr synaptic terminals are symbolized by large and small filled circles,vely. Same scheme as in Fig. 1, supplemented by reciprocal inhibitionxor group Ia fibers to extensor -motoneurons, and vice versa. Note thatal Ia inhibitory interneurons (Rec Ia inh IN) mutually inhibit each other.

ay, is debatable (Section 9.4.8.3). In any case, such rea-puts recurrent inhibition in close functional associatione stretch reflex. Moreover, recurrent inhibition appears tovolved together with mammalian muscle spindles, theirof two afferents and -innervation [158,387,391].ther functional association between recurrent inhibi-d the muscle proprioceptive system may be construed

ows. Skeletal muscles generate movements by develop-ces against the prevailing loads, entailing muscle-lengthint-angle changes. Changes in muscle length in turn co-ine muscle force via the well-known forcelength andvelocity dependencies [279]. For control purposes, theseportant state variables had best be fed back to the cen-

ntrollers. In addition, muscle force is determined by itsion via -motoneurons. Thus, in a recent model of themusculo-skeletal system of the cats hindlimb, Loeb et6,217] suggested that -motoneurons receive feedbackof three pertinent state variables: muscle force, muscle

and an estimate of muscle activation. In this scheme, Ren-ells were suggested to provide an efference copy of motorused to estimate the muscle activation or force componentted by neural excitation [216,217,388391].ortance of muscle spindles for posture and movementy been underscored by neurotrophin-3-deficient miceable to support their weight and exhibit unnaturale to an absence of muscle spindles and proprioceptivetheir limbs [93,375].

nown reasons, some classically decerebrate prepara-temporarily exhibit rigidity predominantly in flexorurthermore, in the acute spinal cat, the injectionxy-phenylalanine (DOPA) may enable tonic stretchoth flexor and extensor muscles [239]. Finally, whilea slippery surface (e.g., ice), humans assume a safety

which they stiffen their legs by extensor-flexor co-It may thus be expected that monosynaptic reflexo exist in limb flexor muscles, which is the case.

rocal Ia inhibition

re situations when flexor muscle activity has to bewith extensor activity. If a perturbing stretch of an

uscle elicits its autogenetic reflex contraction, thisch the antagonist muscle(s) and elicit an antagonistex. In order to prevent this from happening (whichto a cascade of agonistantagonist contractions),

rons to antagonist muscles should be reciprocallyimultaneously with the stretch-evoked activation of

schematically illustrated in Fig. 2, a second impor-connection of muscle spindle group Ia afferents isntal lamina VII interneurons that inhibit antagonistrons (and some cells of origin of the ventral spino-ract (VSCT), not illustrated) [164].cal inhibition may have an undesired side effect.nsor muscles are activated and shorten, the antag-r muscles are stretched. Thereby flexor groups increase their firing rate, excite their homony-otoneurons and reciprocally inhibit the extensorrons, which may interfere with the extensor actionalternating movements, in particular. This side effectvented by in turn inhibiting the flexor-coupled Ias by their opponents, introducing mutual inhibitiontual inhibition is a fairly common mechanism amongopulations of spinal interneurons [18,164,165,329].

rent inhibition

eding discussion might suggest that, quite generally,on of one neuronal circuit may create a side effectoval would call for another circuit. Along this line, recurrent inhibition has been suggested to solve atroduced by reflex actions of muscle spindles and theirontrol. Thus, recurrent inhibition has been hypothe-

calize the stretch reflex [37], to counteract the effectsons in fusimotor bias to muscle spindles [123] or totent of group Ia excitatory effects on -motoneuronsether, as compared to scientists, evolution thinks

Fig. 2. Sevokedized byand theirespectifrom flereciproc

this wsoningwith thhave esystem

Anotion anas folling forand jodetermforcetwo imtral coactivatneuro-

al. [21signalslengthshaw coutputgenera


Another line of research associates recurrent inhibition withanti-gravity functions in stance.

4.3.1. PrevEmphas

recurrent inrefs. [18,17

(i) The sshowsdistalrevealapparevariouand threflexfromferentrecurr

poolsin hanexhibiof othlimb,with aspindlin fineand hdiffereamonggreatehave arole trent ianotheThe drubrosof thereticubution[52].relatedneticvexing

(ii) Withito bepoolsand durecurr

rons ibird [3

(iii) Thereprobainhibition doas exirostro

Simplified diagram of recurrent inhibition. Same scheme as in Fig. 2,ented by recurrent inhibition via Renshaw cells, and mutual inhibitionRenshaw cells. Renshaw cells, which receive their main excitatory

om -motoneurons, inhibit homonymous and synergistic - and -rons, reciprocal Ia inhibitory interneurons excited from homonymousrgistic group Ia fibers, and other Renshaw cells, in particular those pre-tly but not exclusively related to antagonist -motoneurons (mutualn).

Core recurrent inhibitory circuitsschematically illustrated in Fig. 3, intraspinal recurrentaxon collaterals make excitatory synapses on Renshawhich in turn inhibit [18,154,164,178,388,391]:

otoneurons;otoneurons belonging to the same and synergistic -oneuron pools;iprocal Ia inhibitory interneurons receiving monosynap-excitation from homonymous and synergistic musclerents. The functional rationale could be that, since Ren-

cells inhibit -motoneurons, they should also inhibitciated reciprocal Ia inhibitory interneurons with the samep Ia inputs;er Renshaw cells (mutual inhibition) which are par-larly, but not exclusively, related to antagonisticotoneurons;e cells of origin of the ventral spinocerebellar tractCT) receiving monosynaptic excitatory input from groupfferents (not shown).alence of recurrent inhibitionis is here put on the occurrence and distribution ofhibition among limb -motoneurons (for details see8,391]).

trength of recurrent inhibition in the cat hindlimba gradient, becoming weaker in from proximal to

muscles. An even stronger such gradient has beened in the cat forelimb [391]. Such gradients are alsont in humans, where they can be inferred usings techniques based on electrical nerve stimulationeir effects on motor unit discharge patterns and H-

es [178]. The patterns in humans differ somewhatthose in cats, which may be expected from the dif-functional roles of cat and human forelimbs. Thus,ent inhibition is weak or absent in -motoneuronconcerned with precise, distal limb movements, i.e.,d muscles in cat and man [178,391]. This distributionts some interesting associations with distributionser systems. In particular, at least in the cat fore-the distribution of recurrent inhibition is associatedn inverse distribution of -innervation in musclees. The -motoneurons of distal muscles involvedmanipulative movements lack recurrent inhibition

ave a high degree of -innervation, suggesting ant fusimotor regime. Recurrent inhibition is strong-motoneurons of more proximal muscles playing a

r role in posture and locomotion, which muscles alsolower degree of -innervation, relaying a greater

o -fusimotor control and thus associating recur-nhibition with -fusimotor control [158]. There isr association with effects of descending spinal tracts.orso-lateral system consisting of the cortico- andpinal tracts is more important for skilled movementshand, while the ventro-medial system including the

lo- and vestibulospinal tracts make a greater contri-to movements in proximal joints during locomotion

How these correlated distributions are functionallyneeds to be determined. Especially, the phyloge-

persistence of -innervation in mammals remains aproblem for functional interpretation [356].

n this general framework, recurrent inhibition appearsparticularly strong in and between -motoneuronthat are active during the stance phase of locomotionring quiet upright stance. It fits with this pattern that

ent inhibition mediated by Renshaw-like interneu-s present in the chick spinal cord, i.e., in a two-legged79,403].is also recurrent facilitation between-motoneurons,bly mediated via recurrent inhibition of reciprocal Iatory interneurons and of Renshaw cells. This facilita-es not show a topographically organized distribution

sting in recurrent inhibition, and it extends further-caudally [250].

Fig. 3.supplembetweeninput frmotoneuand synedominaninhibitio

4.3.2.As

motorcells, w

-M -M

mot Rec

ticaffeshawasso

grou Oth

ticu-m

Som(VSIa a


5. Muscle proprioceptive feedback and recurrentinhibition in action

So far, tconditions.of muscledynamic m

5.1. Muscl

Duringtendon orgto their res

5.1.1. GolFor the

organs. Sintions, theythe musclepassive forTheir dischto muscleensemblesmuscle weactivity andsurementsensembles[301]. Simrate was higthe amount

5.1.2. MusBy cont

plicated.While i

fusal muscof -motonfreedom, acle spindleare there with theseand structuappear to mterns not creceive inpof this issuconcepts.

5.1.3. FollAfter e

motoneuroengineeringconcept thavation. Inspindle groto homonytem. In slo

inevitable signal-transmission delays around the loop are not thatsignificant, the motor commands descending in the spinal cord

imptiva

-motalsoingsionndlelow

rtonot s-me

theurbaincreflest i

n inponeuwou

stric214

Servumancur

rringassisthatoneu

usc

euroral tendisplie

e disas dyacco

re a

distin

l toto msiredtputer lend byactuvem

s simsum

- a

piteestiotivathe discussion has concentrated on stationary stanceNow the question arises as to the behavior and role

proprioceptive feedback and recurrent inhibition inovements.

e spindles and Golgi tendon organs in action

movements, the inputs to muscle spindles and Golgians change. But their outputs are differently relatedpective inputs.

gi tendon organ discharge in actionsake of comparison, we shall start with Golgi tendonce they are located at the musculo-tendinous junc-respond very sensitively to the forces developed byfibers inserting into them and, to a lesser extent, to

ces developed during muscle stretch [163,299,304].arge in naturally behaving cats appears simply relatedforce [301]. The averaged afferent activity fromof tendon organ afferents from the triceps surae

re fairly well correlated with the electromyographicagreed well with separate triceps surae force mea-

in normal cat locomotion, supporting the notion thatof tendon organ afferents signal whole-muscle forceilarly, in humans, Golgi tendon organ afferent firinghly modulated during active movements, monitoringof muscle force [3].

cle spindle discharge in actionrast, muscle spindle afferent discharge is more com-

n amphibians the activation of extrafusal and intra-le fibers is coupled by -innervation, the existenceeurons in mammals opens up a new dimension of

t least principally. (In some muscle territories, mus-s may also receive sympathetic inputs [309].) Why-motoneurons in addition to - and -motoneurons,classes of motoneurons also having different sizesres [263]? The evolution of -motoneurons wouldake functional sense only if they exhibit activity pat-

losely coupled to those of -motoneurons, and thusuts independent of those to-motoneurons. The studye in animals and humans has led to vividly debated

ow-up length servo hypothesisarly studies on the physiological actions of -ns [123,239], and with the spread of control

ideas in physiology, Merton [253] proposed at was explicitly based on -fusimotor spindle inner-this view, the feedback system set up by muscleup Ia afferents and their monosynaptic connectionsmous -motoneurons would be used as a servo sys-w and precise voluntary movements, in which the

wouldthen acvate couldsupplyexprescle spialso be

Meit did na servo

tion inof diststudiesstretchis moddent o-motwhichsince,grace [

5.1.4.In h

the coin Sheservo-

poses-motfrom mmotontempoceeds uThe imspindlwherevatedto ensulengthsystemparalleposedthe detwo oucle fibsignale

Theing moquite abriefly

5.1.5.Des

the quare acinge primarily on the -motoneurons. These wouldte muscle spindles, which in turn would reflexly acti-oneurons to cause a muscle contraction. This conceptbe applied to locomotion, with the locomotor CPGthe motor command. Mertons idea was an earlyof the notion of internal model, in which the mus-acts as a forward model of skeletal muscle [390] (see). The model was easily understandable.s concept led to much valuable research even thoughtand the test of time. The quality of performance ofchanism critically depends on the power amplifica-loop, that is, the loop gain. For a good suppressionnces, the loop gain has to be high. In subsequentited by Mertons concept, it has turned out that theex gain measured in animals and humans on averagen most circumstances, albeit modifiable and depen-ut amplitude. Moreover, in humans, the activation ofrons was found not to precede that of-motoneurons,ld have been required by Mertons hypothesis. Evert servo control of muscle contraction has fallen from].

o-assistance hypothesisns and animals, many movements are produced byrent activation of both - and -motoneurons, astons standing decerebrate cat (Section 4.1.2). Thetance hypothesis, in its strict version [239], pro-the primary activation of a muscle occurs via itsrons, whose activation is then supported by feedbackle spindle afferents being excited, in parallel, by -ns. The idea is that fusimotor action should provide amplate of the intended movement so that, if this pro-turbed, spindle discharge should ideally be constant.d offset of the effects of muscle length changes oncharge had best be provided by static -motoneurons,namic -motoneurons could be differentially acti-

rding to motor task whenever it would be necessaryhigh muscle spindle sensitivity to imminent muscle

urbances. This scheme is akin to a model-referencewhich an internal model (muscle spindle) is put inthe plant (skeletal muscle) that the model is sup-imic. As long as the movement proceeds according trajectory represented in the fusimotor signal, the

s (intrafusal muscle fiber lengths and extrafusal mus-gths) should match. If not, the difference should bespindle afferents [148,387,390].al discharge patterns of muscle spindle afferents dur-ents in humans and animals have turned out not to beple as required by the servo-asistance hypothesis, asmarized now.

nd -motoneuron discharge patterns in actionmany physiological studies in animals and humans,n of exactly how, during motor acts, -motoneuronsed in relation to -motoneurons has not yet been


settled unequivocally [87,151,265,301]. This is due, in part,to the different movements investigated and different prepara-tions and refrom routinments (respreflex) tohave variedpreparationobtained fror from muinputs coulfusimotor einto staticfusimotor e-innervatithe static intrafusal msome authoeffects viais exploitedis unknownlocomotionof the vario

Studiescles in catcontradictofrom muscmuscles indecreasesand -motoents woulddirect recofire concomremainingterns areanesthetizeincrease thare silenced

Duringrates of mmodulatedtor inputs.depends ontraction duprofiles ofbe predictealone. By cthe tricepsfiles, particthat the cofusal muscbecause thcycle [301]

An impdoes, or dmotoneurosuggested.

outflow to the medial gastrocnemius muscle of high decerebratecats during locomotion, part of the fusimotor outflow (S, type

a temof thrve

thernamoupand63,3umato bspi

hy. Sted rg thlocof intaffexlyrententcree

indlence haffeove

he etretcents

gealplitus m

of monclingleInevikely

thafferes inle, wic or-actinn

enings, ths sh

y, thrge drvo-a

ic futrices ducontvitymuscording methods used. The movements studied rangee rhythmic locomotion and other rhythmic move-iration, mastication), reflex movements (e.g., scratch

voluntary movements. The preparations employedfrom awake, freely moving animals to acute reduceds of various sorts. And the recordings have beenom unidentified or identified -motoneuron efferentsscle spindle afferents in awake cats, where fusimotord be estimated only indirectly. Since, in the cat, theffects on muscle spindles can be functionally dividedand dynamic ones, there are at least four types offfects: static and dynamic -, and static and dynamicon (the dynamic -motor units being of type S and-motor units of type F), mediated via three types ofuscle fibers (bag1, bag2, chain fibers). Furthermore,rs suggest a functional division of static fusimotorbag2 and chain fibers [364]. Whether this diversityto the fullest extent under physiological conditions, although this to occur has been suggested for cat[87]. In particular, the selective supraspinal controlus types of -motoneurons is still at issue.performed on respiratory, masticatory and limb mus-s and other animals have yielded diverse, in partry results. During respiration in cats, the dischargele spindles residing in inspiratory and expiratorycreases when their parent muscle is contracting andduring muscle relaxation [65], suggesting that -neurons fire concomitantly, otherwise spindle affer-

be silenced during muscle contraction. Indeed,rdings have shown that - and -motoneurons doitantly, with the exception of some -motoneurons

unmodulated [334]. Similar spindle discharge pat-seen during masticatory movements. In lightlyd cats, spindle afferents from jaw-closing muscleseir firing rate during active muscle contraction, butduring the same movement imposed passively [360].normal locomotion in intact cats, the discharge

uscle spindle afferents from hindlimb muscles aredeeply due to changing muscle length and fusimo-In addition, the precise spindle discharge patternthe particular parent muscle and its type of con-

ring movement [213,265,299,301]. The firing ratespindle afferents from hamstring muscles could

d fairly well from the length and velocity signalsontrast, the firing profiles of spindle afferents fromsurae muscles deviated from the predicted pro-

ularly during electromyographic activity, indicatingmponents of fusimotor action correlated with extra-le activity were significant in triceps surae, possiblyis muscle is more strongly recruited in the cat step.

ortant question is which type of fusimotor neuronoes not, modulate its discharge in parallel to -ns. A number of combinatorial patterns have beenFor example, in some cases, such as the fusimotor

1) haseningthus sewhile othe dythe grening[362,3

In husuallymusclerograprestricardisinduringings ospindleor refleIa affemovem

scope sthe spassistaspindlewith mfrom tited a smovem

phalanilar amspindlements

In cof a s[214].most lactionsthat dipatternexampof statwith musclelengthIn catmuscleactivitdischathe sedynamas themuscleeningsensitiactiveporal profile resembling the active unloaded short-e parent (medial gastrocnemius) muscle and mayas a temporal template of the intended movement,parts (S, type 2, and D) may serve other functions,

ic -motoneuron (D) pattern possibly sensitizingIa afferents to detect the onset of muscle length-departures from the intended movement trajectory65].ns, modulating inputs to the fusimotor system havee inferred indirecty from effects on the discharge of

ndle afferents, which can be recorded by microneu-uch inferences are usually compromised by a very

ange of movements that can be studied without jeop-e recording stability (virtually excluding recordingsmotion), and by the common inavailability of record-rafusal length changes. The discharges of musclerents show varying patterns during various voluntary

elicited muscle contractions. On the one hand, groupdischarge hardly changed during a precision fingerthat tracked a trapezoidal waveform on the oscillo-n and caused length changes of the muscle containing[152]. This is in keeping with Matthews servo-

ypothesis (Section 5.1.4). On the other hand, musclerents have been seen to modulate their discharge ratement. For example, most muscle spindle afferentsxtensor digitorum muscles of the forearm exhib-h response while the subjects performed alternatingof moderate speed at the appropriate metacarpo-

joint, and in response to imposed movements of sim-des and velocities. Hence, in general, human muscleonitor muscle length and velocity in routine move-oderate speed as long as opposing loads are small [3].usion, simple schemes, such as the servo-regulationmuscles length or stiffness are no longer viable

itably, more complex concepts are called upon, whichneed to take account of the diverse biomechanical

t different muscles may have. It is well conceivablent motor tasks require different fusimotor activation

relation to skeletomotor activation patterns. Forhether during rhythmic movements the dischargedynamic -motoneurons is rhythmically modulatedivity may be functionally related to whether theervated by them undergoes shortening (concentric),

(eccentric) or near-isometric contraction [265].e masseter, medial sartorius and tibialis anteriororten when active and receive phasic static fusimotorus maintaining or increasing group Ia afferentepending on shortening velocity in accordance withssistance hypothesis. On the other hand, phasicsimotor activity has been observed in muscles suchps surae during locomotion and external intercostalring respiration, these muscles undergoing length-ractions while active. Increased dynamic spindlecould then counteract lengthening by supporting thecle via the monosynaptic Ia afferentmotoneuron


connection. The function of tonic fusimotor discharge patternsis less clear [265].

5.1.6. Sup-motoneu

Since skeletal mdescendingfullfil theirtional descvestibulo-,mono- or ppatterns deposition (etype [36,52descendingated via cecutaneousthere are cbic systemnuclei, theand serototems [52,10receive dirall groups (charge pattthey, too, mthose of -

5.2. Moduinhibition

While mappear tosophisticatmotor taskcally ancienamely pregic internedepolarizatgive rise t[18,154,16

Relatedsynaptic efcutaneous

State- aAs comptransmispressed bwith, pertor activsuch asThis depspindle aH- and s

implified diagram of influences exerted by groups IIIIV afferents fromr muscles on spinal moto- and interneurons. Also included are some path-m extensor group Ib afferents from Golgi tendon organs, which during

ibit extensor -motoneurons and facilitate flexor -motoneurons (viary and excitatory interneurons, respectively), while during the stancecilitating extensor -motoneurons via excitatory interneurons, whichart receive convergent group Ia afferent inputs (for details see text). Forty, spindle group II afferents have been omitted. Furthermore, interneu-diating presynaptic inhibition of sensory afferents are indicated by filledenoted PS. Group IIIIV afferents are symbolized by black dottedlines and may have oligo- and polysynaptic, excitatory or inhibitory

for details see text). Abbreviations: PS, interneurons mediating presy-hibition; RC, Renshaw cell.

se-related locomotor-related modulation. Presynapticbition also varies phasically throughout the locomotore [317].sory-evokedmodulation. Rhythmic modulation of afferentt during natural locomotion also modulates presynapticbition [317].raspinal modulation. Signals descending fromaspinal sources may contribute to the phasic modulationresynaptic inhibition [317]. Among the rhythmically

ve supraspinal neurons are brainstem (reticulo-, rubro-,ibulospinal), cerebellar and cerebro-cortical cells [12].raspinal and sensory inputs to - androns-motoneurons communicate the CNSs commands touscles, they must receive all kinds of inputs from

tracts and sensory afferents (Fig. 1) in order tomultifarious roles in various motor acts [18]. Tradi-

ending systems include the cortico-, rubro-, reticulo-,tecto- and interstitiospinal systems, which terminateolysynaptically on -motoneurons in differentiatedpending on muscle type (e.g., flexor or extensor),.g., proximal of distal in limb), and motor unit,373]. In cats, monkeys and humans, parts of thecommands to forelimb -motoneurons are medi-

rvical propriospinal interneurons, which also receiveand muscle afferent signals [5,6,290]. Furthermore,omplex descending pathways arising from the lim-, hypothalamic nuclei, locus coeruleus and raphelatter two exerting neuromodulatory noradrenergicnergic effects on various spinal neuronal sys-8,144,162] (Section 7.2.3). Finally, -motoneurons

ect or indirect projections from sensory afferents inIIV) (see below). Since -motoneurons exhibit dis-erns that in part diverge from those of-motoneurons,

ust receive various inputs that differ in part frommotoneurons [151,387].

lation of segmental sensory input by presynaptic

uscle spindle feedback during movement mightbe controlled, by fusimotor systems, in a way

ed enough to subserve varying demands of variouss, it is further complicated by a phylogeneti-nt system at its very entrance to the spinal cord,synaptic inhibition, acting via inhibitory GABAer-urons (see Fig. 4) and producing primary afferention in sensory afferent terminals, which may at timeso antidromic action potentials in sensory afferents4,317,318,329,383].to locomotion, presynaptic inhibition modulates theficacy of spindle group Ia and II, tendon organ Ib andafferents [317,351]:

nd task-dependent locomotor-related modulation.ared to non-locomotor states in cats, the synaptic

sion from group Ia afferents to-motoneurons is sup-y an augmented tonic presynaptic inhibition, startingsisting throughout and outlasting the fictive locomo-ity [121]. This also holds for other sensory afferents,those from muscle spindle group II afferents [248].ression of synaptic transmission in group Ia and IIfferent pathways may contribute to the reduction oftretch reflexes during locomotion [317].

Fig. 4. Sextensoways frorest inhinhibitophase faalso in psimplicirons me

circles darrowedeffects (naptic in

Phainhicycl

Seninpuinhi

Supsuprof pactivest


The descending tracts have effects not only on - and-motoneurons, but also on spinal interneurons, amongwhich arIn humwith chamagneticmodulathuman lIn monkinhibitiobut notof descemoveme

Note thaulations thafferent senrecorded, h

5.3. Recip

The strantagonisthas been sparadigms,[66,153,15reciprocal i

Duringdriven by tduring theing decerebgroup Ia inthe stancemotoneurothe same gthe pharmastrychninethey do noinhibition i

In humamuscles delocomotorin line withtion is rhytexerting sm[208,272,2movement,is decreaseinhibition osilence andstretch [272

Part ofduring locis the case(Section 5.2tically exciinterneuron

cats walking on a treadmill, a large subset of vestibulospinal neu-rons modulate their discharge rhythmically around a substantial

rate,uralor acicityxtenally,omoion (orybitor

rolnistshavetractshou

umm

ion o2), bentscorts iniuteby mstibuterisnver

cult

ecur

strehis

l m78,3

Recuce thoneuurings theat fiin

oneuor

euront inthat274,eric

8,38apticurone those mediating presynaptic inhibition [154,164].ans, voluntary ankle movements are associatednges in presynaptic inhibition [155]. Transcranial

stimulation of the motor cortex differentiallyes presynaptic inhibition of group Ia afferents inower limb (depression) and arm (increase) [254].eys, sensory afferent terminals receive presynapticn from descending tracts (e.g., pyramidal tract),vice versa, which might help preserve the qualitynding motor commands during centrally initiatednts [161].

t it is usually the compound effect of all these mod-at determine the pattern of presynaptic control ofsory inputs, this compound action mostly not beingowever [317].

rocal inhibition in action

ength of disynaptic reciprocal inhibition between-motoneuron pools depends on the motor task. Thistudied in humans and animals, using several motor

including locomotion and voluntary movements4,261,272,329]. Here emphasis is put on changes ofnhibition during locomotion.

locomotion, reciprocal Ia inhibitory interneurons arehe locomotor CPG and their group Ia afferent inputstimes when their muscle is active [317]. In walk-rate cat preparations, Ia inhibitory interneurons withput mainly from quadriceps fire maximally duringphase [95]. During fictive locomotion in the cat, -ns and reciprocal Ia inhibitory interneurons receivingroup Ia afferent input are active concurrently. Sincecological blockade of the latters output synapses bydoes not interrupt the locomotor rhythm, however,t belong to the locomotor CPG [298]. Reciprocal Ias also operative during fictive scratching [39].ns, reciprocal inhibition between ankle antagonist

creases from quiet stance via walking to running, withspeed being the major determinant [184]. Moreover,

the above cat data, disynaptic reciprocal Ia inhibi-hmically modulated during walking and bicycling,all effects on the muscles being active in a phase

88,306]. The present view is that, during voluntarythe disynaptic Ia inhibition of the agonist muscles

d to facilitate their action, while the disynaptic Iaf the antagonist muscles is increased to ensure theirsuppress stretch reflex activity resulting from their].the rhythmic modulation of reciprocal inhibition

omotion may derive from supraspinal sources, asfor interneurons mediating presynaptic inhibition). For example, the vestibulospinal tract monosynap-

tes extensor motoneurons and reciprocal Ia inhibitorys projecting to antagonists [153,154]. In decerebrate

mean

to postextensrhythmlarge e

Fining locinhibitinhibitIa inhi

Theantagosome

co-con

that it[268].

In sinhibittion 4.movem

ing thereflexecontribmentsand vecharacsive coso diffi

5.4. R

Thetask. Tsevera

[154,1

5.4.1.Sin

-motcally dneuron

In culated-motflexionmotonrecurre

catingCPG [

Undrhythm[18,17presyninternewhich consequently contributes a tonic backgroundsupport [277]. Thus, these neurons contribute to thetivity in an appropriate phase-dependent way. Theof vestibulospinal neuron discharge originates, to a

t, from the cerebellum [12].part of the modulation of reciprocal inhibition dur-tion may also be due to modulation of presynapticSection 5.2) of group Ia terminals on reciprocal Ia

interneurons or, possibly, of terminals of reciprocaly interneurons on -motoneurons [92].e of reciprocal inhibition in the co-contraction ofto stabilize a joint is somewhat controversial. Whileargued that reciprocal inhibition is reduced duringion [66,154], there is also some evidence to indicateld play an important role in increasing joint stiffness

ary, it has been shown that Ia interneurons mediatef antagonists not only during muscle stretches (Sec-ut also during centrally induced fictive locomotion,commanded by several descending systems includ-

icospinal tract, crossed extensor reflexes, and posturaltiated from the vestibular system [165]. They alsoto the coordination of left and right hindlimb move-ediating part of the crossed inhibition from reticulo-lospinal tracts [167]. This multi-functionality is a

tic of other spinal interneurons and requires a mas-gence of various inputs, which makes their workingsto understand.

rent inhibition in action

ngth of recurrent inhibition depends on the motorhas been studied in humans and animals, using

otor paradigms, including voluntary movements87,391]. Emphasis is here put on cat locomotion.

rrent inhibition in cat ctive locomotione main excitatory input to Renshaw cells derives fromrons, their discharge should be modulated rhythmi-locomotion and transfer this modulation to follower

y inhibit.ctive locomotion, Renshaw cell discharge is mod-phase with activity of their main input-givingrons, that is, most of them are active during eitherextension when their predominant excitatory -

n pool is active [249]. Pharmacologically blockinghibition does not disrupt the locomotor rhythm, indi-Renshaw cells are no integral part of the locomotor298].natural conditions, Renshaw cells may receivemodulating signals also from descending tracts7,391], as is the case for interneurons mediating

inhibition (Section 5.2) and reciprocal Ia inhibitorys (Section 5.3).


5.4.2. Recurrent inhibition of reciprocal inhibition in catctive locomotion

Since Rinterneurontion might blocomotingat the end oreciprocalrate [298].

More getion of recireciprocal icles are tofine explormuscles isrole of recistabilize a

5.5. Compnonlinearit

Duringpropertiestake care oOne set oflinearities(Section 5muscle act

5.5.1. LineWhen in

by a ramp-the muscleelasticity ohas only acontinuingcle is shortnegative sithe formeroperating rand, morelinearizatiotion by thelarger thanby electromcontributesening (ecce

Based odiscarded l5.1.3) and smuscle forregulate stian elastic schange ovecle spindlewhile forcefed back n

combined action of both autogenetic feedback systems wouldprovide for stiffness regulation.

con

deceor theninges, inht noe imfleximp

ctionmentextenwalkwn

b hablis

almd sevsura

ointtretc

Copnshimm

ric cnto all-knFore v

becon

ningcentrmotstret-acticands tot a lo

Comtheron-u

ing ediffengleat thevel.s fro

ts mongle.ermiivatienshaw cells inhibit related reciprocal Ia inhibitorys (Fig. 3), the formers rhythmic discharge modula-e reflected in the latters discharge. In fact, in fictivelycats, when extensor Renshaw cells increase their ratef the extension phase, most of the quadriceps-relatedIa inhibitory interneurons decrease their discharge

nerally, it has been proposed that the recurrent inhibi-procal Ia inhibitory interneurons may serve to reducenhibition if the contraction forces of antagonist mus-be finely balanced, for example during alternating oratory movements, or if co-contraction of antagonistrequired [154,329]. As noted above (Section 5.3), theprocal inhibition in co-contraction of antagonists tojoint is somewhat controversial, however.

ensation for muscle properties and jointies

movement, a number of problems arise from theof musculo-skeletal systems, which the CNS has tof and may do so by using proprioceptive feedback.problems relates to muscle properties, such as non-(Section 5.5.1), forcelengthvelocity relationships.5.2) and muscle fatigue (Section 7), the other toions on joints.

arization of muscle stiffnessa decerebrate cat an active soleus muscle is extended

and-hold stretch, force first increases steeply, due tos intrinsic stiffness, which is commonly attributed tof existing acto-myosin crossbridges. This elasticityshort range of operation, which when exceeded bystretch causes the muscle to yield. When the mus-ening using the same ramp-and-hold stretch but ofgn, the fall in force is more dramatic than the rise incase, in particular due to the lack of yield. With aneflex loop, both force responses become enhancedimportantly, more symmetrical to each other. Thisn is due to asymmetric changes in muscle activa-reflex. The activation induced by stretch is muchthe de-activation induced by release (as measuredyographic activity), implying that the stretch reflexmost to muscle mechanical responses during length-ntric) contractions [269].n results such as those described above, Houk [147]ength-servo hypotheses such as Mertons (Sectionuggested that, rather than regulating muscle length orce as individual variables, the stretch reflex serves toffness as a compound variable. In physics, stiffness oftructure (e.g., a spring) is defined as the ratio of forcer length change. Length would be signaled by mus-afferents and positively fed back to -motoneurons,would be signaled by Golgi tendon organs and be

egatively to -motoneurons (see Section 5.6). The

Thein thesible flengthspindlthe rigdict ththeir re

Ancontraexperianklewhileing dohindlim(re-estwalkedshowetricepsankle jlocal s[1].

5.5.2.relatio

Asyeccenttaken ithe we[279].the samshouldening)(shortethe ecactiveof thetor coprimeappearagains

5.5.3.Ano

from nfollowset ateach away thsame lchangefrom ij

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