Some effects of superior laryngeal nerve stimulation on sympathetic preganglionic neuron firing

URS GERBER AND C.4~10 POEOSA Departnzent of Physiology, ~LicGill C'niversity, Montreal, P.Q., Canada H3G IY6

Received April 5 , 1979

G E R ~ E R , U., and POLOSA, C. 1979. Some effects of superior laryngeal nerve stimulation on sympathetic preganglionic neuron firing. Can. J . Physiol. Pharmacol. 57, 1073-1081.

Repetitive electrical stimulation of adrerent fibers in the superior laryngeal nerve (SLN) evoked depressant or excitatory effects on sympathetic preganglionic neurons of the cervicai trunk in Nembutal-anesthetized, paralyzed: artificially ventilated cats. The depressant effect, which coilsisted of suppression of the inspiration-synchronous discharge of units with suck firing pattern, was obtained at low strength and frequency of stimulation (e.g. 600 mV, 30 Hz) and was absent at end-tidal COz values below threshold for phrenic nerve activity. The ex- citatory etTect required higher intensity and frequency of stimulation and was CQ2 independent. The depressant effect on sympathetic preganglionic neurons with inspiratory firing pattern seemed a replica of the inspiration-inhibitory efTect observed on phrenic motoneurons. Hence, it could be attributed to the known inhibition by the SLN of central inspiratory activity, if it is assumed that this is a common driver for phrenic motoneurons and some sympathetic pre- ganglionic neurons. The excitatory effect, on the other hand, appears to be due to connections of SLN afferents with sympathetic preganglionic neurons, independent of the respiratory center.

GERBER, U., et POLOSA, C. 1979. Some effects of superior laryngeal nerve stimulation on sympathetic preganglionic neuron firing. Can. J. Physiol. Pharmacol. 57, 1073-1081.

Une stimulation klectrique repetitive des fibres afferentes du nerf laryng6 sup6rieur (SLN) evoque des effets dkpresseurs ou excitateurs sur les neurones sympathiques prkganglionnaires du tronc cervical chez des chats anesthesiks au Nembutal, paralysks et ventilb artificiellernent. 1,'effet depresseur consiste en la suppression des decharges symchronis~~s h l'inspiration des unites presentant ce genre de patron de dkcharge: ceci est obtenu pour des stimulations de faible amplitude et de basse frequence (par exemple: 600 rnV et 30 Hz), et n'apparalt pas, pour des valeurs de C 0 2 mesurees en fin de respiration courante inferieures h cellss dkclenchant llactivitC du nerf phrenique. L'effet excitateur nkcessite une stimulation plus grande en intensitd et en frequence et ne dkpend pas du CO2. L'effet dkpresseur sur les neurones sympathiques prC- ganglionnaires presentant un patron de dkharge lie B l'inspiration, semble Ctre une rkplique de 19effet inspiratoire inhibiteur observk avec les motoneurones phrkniques. On peut pour cela attribuer cet effet B l'inhibition connue de l'activitk centrale par le SLN, si 1'011 adrnet qu'il s'agit d'un conducteur partagk par les motoneurones phrkniques et quelques neurones sympathiques prCganglionnaires. D'autre part, l'effet excitateur semble Ctre dO B des connexions d'affgrences du SLN avec des neurones sympathiques prkganglionnaires qui ne dependent pas du centre respiratoire.

[Traduit par le journal]

Introduction CIA (monitored by recording phrenic nerve ac-

Previous work on the background firing patterns of cervical trunk SPNs (Mannard and Polosa 1973; Preiss et al. 1975) led to the identification of a population of SPNs that fire either exclusively during inspiration or throughout the respiratory cycle, but attain peak firing frequency during iinspiratisn. These units have been labelled "inspiratory" SPNs (Preiss et al. 1975) and represent half of the SPNs with background activity found in the cervical sym- pathetic trunk.

The time relation of the firing of these units to

tivity) and the modifications of their firing by changes in arterial CQ2 or by lung inflation, suggest that CIA is the source of the inspiration-synchronous activity of these units (Preiss et al. 1975; Preiss and Palosa 1977; Gerber and Polosa 1978). It slnould be expected therefore that any procedure that sup- presses CIA or produces phase shifts in its rhythm would alter the firing pattern of inspiratory SPNs in a selective and predictable manner.

In the present experiments we have tested this prediction by studying the effects of electrical stim- ulation of a group of low-threshold afferent fibers in

ABBREVIATIONS: SPN, sympathetic preganglionic neuron; the SLN. ~ h & e afferents, which have their receptive

CIA, central inspiratory activity; SLN, superior laryngeal in the the upper tract nerve. (Sampson and Eyzaguirre 1964; Boushey et al.

0008-4212/79/101073-09$01.00/0 @ 1979 National Research Council of Canada/b=onseil national de recherches du Canada

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1071 CAN. J. PE%YSI[O%. PHARMACOL. VOL. 59, 1979

19941, have a cl~aracteristic inspiration-inhibitoq and expiration-excitatory effect. Repetitive stirnula- tion of these afferents in spontaneously breathing animals invariably causes apnca (Rosenthal 1862; Han~mouda and !Vilssin 1935; Millenbrand and Boyd 1936; Larrabee and Modes 1948 ) . Behaviourally, the apnea may be considered a component sf the swallowing reflex (hIiller and Lsizzi B 974 1. We pre- dicted that SLN stimulatic~n would selcctively dcpress the firing of inspiratory SPNs. We also predicted that if SLN stimulation could produce phase shifts in CIA and a tight coupling existed between brain- stem inspiratc~ry neurons and SPNs. similar phase shifts would be observed in the activity cycle sf inspiratory SPNs. The experiments have confirmed these predictions. In addition, wcak excitatory effects of SLN stimulation on SBN activity were also found. Tlnese excitatory effects were obtained with higher intermsity and frequency of sthmulation than those required to cause inspiratory inhibition.

Methods Twenty cats were anesthetized with Na pentobarbital in-

traperitoneally ( 3 5 mg /kg), paralyzed with gallamine tri- ethiodide (8 ~ n g kg h-"1, tracheostornized, and ventilated with a positive-pressure respiratory pump. An artery and a vein were cann~~lated for recording systemic arterial pressure and for administering drugs. BiIateral pneumothorax and vagotorny low in the neck were perfornned in most cats. Body temperature was maintained at 36-39°C by means of a heat- ing pad and infrared lamp. End-tidal C 0 2 uras monitored with a Beckman LB3 analyzer and ventilation adjusted to obtain values between 3.5 and 4.5%. The phrenic nea-ve, the internal branch of the Sf-N (Miller and Branmire 19461, and small strands of the cervical sympathetic trunk were dis- sected free of connective tissuc and p l a ~ e d on bipolar silver hook electrodes in a pool of paraffin oil. The nerve signals were amplified, displayed on an oscilloscope, and stored on magnetic tape. Phrenic nerve action potentials were half- wave rectified and integrated with a "'leaky" RC circuit (tirne constant 100 111s). The SPN running average fleqi~ency was csrnputed by a gated pulse counter. Central inspiratory ac- tivity was srappressed by electrical stimralation of SLN affer- ent fibers with trains of square pulses, 0.1 rns im duration, at frequencies of 30-80 Hz. Stimulus intensities (600-800 nnV) just sulticient to abolish phrenic nerw activity were used. Excitatory effects of SLN afferents on SPNs were inves- tigated by stim~~lation of the afferents with double or triple shocks, 0.1 111s in duration at 200 Hz and intensities of 1.0-1.5 V. Inspiration is defined here as the time interval from the onset crf phrenic nerve activity to the start of rapid decrease in activity, determined from the integrated phrenic neua-ogram. Expiration is the interval between termination of one inspiration and the onset of the next.

Eflects of SLN Stimulatioaz on Phrenic Nerve Activity Repetitive stimulation of the SLN for 20-20 s

(see iVethods for stimulus parameters ) always

abolished phrenic nerve activity. In nearly all eases the effect lasted for the entire duration of stinlulation (Fig. 1 A and B, and Fig. 4) . Occasionally phrenic nerve activity resumed just before the end of stimula- tion (Fig. 6 A) . If the onset of the stimulus train occurred while a phrenic burst was in progress, tbe burst was considerably shortened (Fig. 1 A and B, Fig. 2 A, and Fig. 4 A and B) . Tlne SLN was also stimulated with shorter trains of stimuli ( 100-200 ms, same parameters as above) at different phases sf the respiratory cycle. With this procedure, easily detectable changes in respiratory rhythm could be prc~duced. Trains delivered in expiration prolonged this phase, resetting the respiratory rhythm (Fig. 5A). Trains arriving during inspiration shortened the phrenic ncrve b~arst. In about half the cases, the following inspiration was advanced, i.e. a reset sf the rhythm had occurred. Exceptions were one case in which trains delivered during the first 2096 of expira- tion caused the appearance sf an additional, short, phrenic nerve burst, and two eases in which stinlulus trains given in inspiration prolonged the phrenic burst and delayed the next inspiration (Fig. 5 6 ) .

Eflects of SLN Stimulation on SPN Activity SLN stimulation had complex effects on SPN

firing. With repetitive stimulation: the iarost striking effect was a suppressio~l of the respiratory-modulated firing of inspiratory SPNs, paralleling the suppression of phrenic nerve activity. However, in some lanits a slight increase in the rate of nonmodulated back- ground firing was observed, indicating the existence of a weak excitatory pathway fronn SLN afferents to cervical trunk SPNs. These excitatory effects were best studied by stimulating the SLN afferents with double or triple shocks at intensities higher than those used for suppressing phrenic nerve activity. The responses of SPNs to activation of the two types of SLN input will be described separately.

Repetitive Siimukatio~a: Eflects on lazspiratory SPNs

As defined in the %ntroduction, "inspiratosy" SPNs are those which show the highest probability of firing in inspiration (Pseiss ct al. 1975 ) . Depend- ing on whether or not they fire in expiration, their firing patterns have been further subdivided into "continuous with inspiratory peak" and ""brsty." Repetitive stiinulation of the SLN, with the same stimulus parameters that cause suppression of phrenic nerve activity. abolished the inspiration-syra- chrono~rs activity of all seven "bursty" SPNs studied. Ttvo examples are shown in Fig. 1 . One unit was completely silent throughout the period of SLN stim- ulation (Fig. BA) . Six units showed an initial silence,

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GERBER AND POLOSA

FIG. 1 Suppression of firing s f "inspiratsry" SPNs by electrical stimulation sf the SLN. From top: stimulus, SPN spikes, integrated phrenic neurogram, systemic arterial pressure. (A) and (B) are two different units.

of variable duration, followed by the appearance of continuous, irregular firing at mean rates well below control values (Fig. 1B). For the seven "bursty" units studied, the mean firing rate was reduced, during SLN stimulation, from 2.8 0.7 to 0.8 -t 0.2 spikes/s (mean t SEM) . This differ- ence is significant at B < 0.085 (paired t test, Snedecor and Cochran 1967 ) .

Six units with the firing pattern defined as "con- tinuous with inspiratory peak" were studied. During repetitive SLN stimulation the inspiratory peaks in their firing were abolished but the units continued to fire (Fig. 2). Their mean firing rate decreased from 6.7 t 1.4 to 5.7 k 1.3 spikesls (B < 0.05). A comparison of the two units of Fig. 2 shows that the degree of depression of firing rate depends on the intensity of respiratory modulation. Also from Fig. 2 it can be noticed that the firing of these units, during SLN stinlulation, approached the level recorded, in control conditions, during the expiratory phase. The exception was one unit that fired at a higher mean rate during SLN stimulation than in

control conditions. If SLN stimulation reduces SPN firing rate in-

directly by suppressing a portion of their facilitatory input (disfacilitation) , the extent to which SPN firing rate is reduced should vary with the proportion of the excitatory drive provided by the inputs that are depressed by SLN stimulation. As a major excitatory input to inspiratory SPNs is related to CIA and this seems to be the input depressed by SLN stimulation, increasing the CIA itself should increase the apparent effectiveness of SLN stim- ulation.

Figure 3 shows the response of an SPN to SLN stimulation during ventilation with 4 and 7% C 0 2 in 02. At the highest C 0 2 level, when CIA was greatest, as shown by the height of the peak of the integrated phrenic neurogram, SLN stimulation ap- peared to cause the greatest reduction in SPN mean firing rate. Conversely, suppression of CIA by hyper- ventilation in air (end-tidal C 0 2 1.5 % ) eliminated the depressant effect of SLN stimulation on inspir- atory SPNs (Fig. 4) .

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CAN. J . PHYSIOE. PHARMACOL. VOL. 57, 1979

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FIG. 2. EfFect of SLN stimulation on "inspiratory" SPNs which fire both in inspiration and expiration. From top: SPN spikes, stimulus, ratemeter record, integrated phrenic neurogram, systemic arterial pressure. (A) and (B) are two tiitrerent units. Notice during stimulation suppression s f only inspiratsry firing peaks of the unit and persistence of firing at a level close to control expiratory level. Unit A has the greatest i~lspiratory peaks and the greatest depression on stimula- tion.

Finally, whenever SLN sth~ulation caused changes of the SLN was the decrease in mean firing rate sf in duration or frequency of the CIA, these were inspiratory SPNs, described above, due to the sup- always accompanied by similar changes in the pression of the inspiration-synchronous component inspiration-synchronous activity of SPNs (see Figs. of their activity. However, in some units repetitive 1B and 5 ) . SEN stimulation produced other changes in firing

Repetitive Stimulation: Eflects on SPNs Dis- charging witJzuut Respiratory Modulation

SLN had variable effects on the nine units sf this type that were steadied. Four units showed no change in firing rate during stimulation (Fig. &A), one unit showed an increase, and the remaining four units showed a slight decrease that lasted only for the first few seconds of stimulation (Fig. 6B). For this group of units the mean firing rate was reduced from 1.25 A (11.32 to 1.21 & 0.41 sgikesjs. Thcdifference is statistically insignificant. In all these cases, SEN stimulation was effective in suppressing CIA, as show11 by the abolition of phrenic ncrve activity.

pattern that indicated the existence of an excitatory pathway from SLN afferents to SPNs. For example, six units of the burst type had a mean firing rate during stirnulation that was higher than their control firing rate in expiration (i.e. in the absence of CIA, see Rcsults, p. 1075). In another respiratory unit, the mean firing rate during stimulation even exceeded the control rate in spite of the loss of the inspiration- synchronous component of its firing (see Results, p. 1075 ) . An increase in firing rate was also seen during stimulation in one unit that did not receive an inspira- tion-synchronous input (see Results, p, 1076).

The excitatory effect of SEN stimulation was studied in some detail in five units. Trains of two or

Dou b He- and Triple-shock Stirnu Eation three stimuli (see Methods for stimulus parameters) The most striking cff w t of repetitive stimulation were eased as single shocks were ineffective in evoking

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GERBER AND POLOSA I077

Fro. 3. Effect of SLN stimulation on "inspiratory" SPN at two levels of end-tidal C02. From top: stimulus, SPN spikes, ratemeter record, integrated phrenic neurogram, systemic arterial pressure. End-tidal COz 47; in (A), 7% in (B)

spike discharges. The trains were repeated at 3-s intervals. Three of these units were inspiratory and were studied in hypocapnia (end-tidal C 0 2 1.5 % ) in order to eliminate their burst firing. The two non- modulated units were studied in normocapnia (end- tidal CO, 4 % ) . Stimulation evoked spikes in all these units. The tl~reshold stimulus intensity was 1.1 V (2.0-1.4). Latency was variable. Average min- imum latency was 98 ms (range 3 5 - 2 0 ) . Less than half of the stimulus trains evoked spikes; the average firing index (number of action potentials evoked by one stimulus train) was 0.4 (0.3-0.7).

Discussion The effects of SLN stimulation on SPNs, observed

in the present series of experin~ents, can be classified into three main types. The first, and the one that we predicted, was a selective suppression of that portion of SPN activity which is time locked to inspiration (Figs. 1 ,2, 3, and 4) . This effect was seen in 1 3 cells. This effect is maximal on SPNs with the highest in- tensity of respiratory modulation (burst units). It is absent at low end-tidal C02 values and increases in magnitude with increases in C 0 2 values above normal. These properties suggest that the depressant effect is the result of a suppression of CIA by SLY stimulation. If CIA were the main source of excita- tion for inspiratory SPNs (Polosa et al. 1977) a dis-

facilitation of these neurons would result. Evidence that SLN stinlulation acts on the mecharmisms gen- erating rhythmical inspiratory activity is provided by the observation that brahstenn inspiratory neurons are de,pressed by SLN stimulation (Sessle et al. 1 974 ) and by our observations that SLW stimulation causes phase shifts in the rhythm of phrenic nerve activity. The latter effect could not be explained by a direct action of SLN afferents on phrenic mots- neurons. The second effect was a depressioia of SPN activity not related to inspiration. This effect was seen in four cells only and was of snlall magnitude (Fig. 6B). This effect can be attributed to an in- hibitory connection of SLN afferents either onto the SPNs or onto antecedent neurons that are involved in the mechanism of generation of the tonic activity of SPNs. In the conditioils of our experiments, the changes in neuron pool output due to this effect were negligible. The third effect was an excitation. This effect was studied in some detail in five units, but was present in several other units. At the intensity and frequency of repetitive SLN stimulation used in most experiments, i.e. just sufficient to cause sup- pression of inspiration, the excitatory effects were weak and concealed, at least as far as inspiratory SPNs were concerned, by the more easily detectable depressant effects.

I t is of interest that some investigators have

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CAN. J. PHYSIBL. PHARMACBL. VOL. 57. 1979

A

- 5 s

FIG. 4. Lack of effect of SLN stimulation when the inspiratory component of a SPN firing is abolished by hypocapnia. From top: stimulus, SPN spikes, ratemeter record, integrated phrenic neurogram, systemic arterial pressure. End-tidal GO 4.5% in (A), 1.5% in (B).

demonstrated cardiovascular responses attributable to sympathetic excitation (increase in arterial pres- sure, increase in total vascular resistance) by natural stimulation of receptors with afferents in SLN (Nadel and Widdicombe 1962; Tomori and Widdicombe 1969). These reflex responses have been found in decerebrate, unanesthetized animals and have been found to be greatly attenuated or abolished by anes- thesia (Nadel and Widdicombe 1962). The pento- barbital anesthesia, used in our experiments, might have weakened the excitatory effects mediated through SLN afferents, making the depressant effects dominant. It is possible that if the experiments had bcen done without anesthesia, o r with anesthetics other than pentobarbital, the balance between the excitatory and the depressant effects might have been different. The sampling might also have been biased, as pointed out above, by the choice of stimulus parameters, which, with the exception of the ex- periments devoted to studying the properties of excitation, were just adequate to cause suppression

of inspiration. Significant phase shifts in the CIA rhythm were

observed when short bursts of SLN stimulation were used (Fig. 5) . The rhythm of inspiratory SPN ac- tivity always changed in the same way as the phrenic. This observation suggests a tight coupling between CIA and inspiratory SPNs.

Previous work (Preiss and Polosa 1977; Gerber and Polosa 1978) has shown that a significant frac- tion of the SPN population has responses similar to those of inspiratory motoneurons under a number of experimental conditions (changes in inspiratory C 0 2 , lung inflation, electrical stimulation of pul- monary stretch receptor afferents in the vagus nerve). The present experiments have shown that the same fraction of the SPN pool responds to SLN stimulation in a fashion similar to phrenic moto- neurons. It seems reasonable to conclude that these SPNs share with the motoneurons of inspiratory muscles an excitatory input from the respiratory center.

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FIG. 5. Short trains of stimuli to SLN evoke similar phase shifts in burst activity of phrenic nerve and of '3nspiratory9' SPN. From top: stimulus, sympathetic neuron spikes, integrated phrenic ncurogram, phrenic neurogram, systemic arterial pressure. (A) Trains in expiration prolong this phase and delay the sympathetic burst correspondingly. (B) First train is Bong and has same effect as in (A). The next two trains occur in inspiration and shorten duration of this phase and of sympathetic burst. ( C ) First and third train occur in inspiration and prolong duration of this phase and of sympathetic burst.

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FIG. 6. Lack of effect of (A), or weak depression by (B), SLN stirnulatioil on firing of nonmodulated SPNs. From top: stimulus, SPN spikes, integrated phrenic neursgram, phrenic neurogram, systemic arterial pressure. (A) and (5) are two ditFerent units.

Acknowledgments This work was supported by grants from the

Medical Research Council sf Canada and the Quebec Heart Foundation. We thank Dr. Laskey for cri- ticizing the manuscript.

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