Presynaptic excitability changes induced in single laryngeal primary afferent fibres

Brain Research, 53 (1973) 333-342

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© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

P R E S Y N A P T I C EXCITABILITY C H A N G E S I N D U C E D L A R Y N G E A L P R I M A R Y A F F E R E N T FIBRES

IN S I N G L E

B A R R Y J. SESSLE

Division of Biological Sciences, University of Toronto Faculty of Dentistry, Toronto 2 (Canada)

(Accepted October 20th, 1972)

SUMMARY

Single neurones were recorded extracellularly with microelectrodes placed in the nodose ganglion of decerebrate cats and cats anaesthetized with chloralose. A total of 106 units were isolated and a laryngeal input was identified in 84 of them. Conduction velocity estimates utilizing SLN stimulation indicated that more than 90~o were associated with small myelinated nerve fibres. An antidromic response could be elicited in the laryngeal units by bipolar stimulation in the region o f their endings in the solitary tract nucleus. A number of these neurones were similarly shown to project to the contralateral brain stem as well. Presynaptic influences on the brain stem endings of these neurones as a result of conditioning stimulation of various cranial nerves were measured indirectly as changes in the level of excitation of the neurones' antidromic responses. Conditioning stimuli applied to the superior laryngeal nerve (SLN), the glossopharyngeal nerve (IX) and the infraorbital nerve (IO) or other orofacial structures were particularly effective in presynaptically depolarizing the brain stem endings of the units. Their effectiveness, plus the onset, peak and time course of the PD, correlate very closely with these features of the inhibitory influences noted in the solitary tract nucleus 27 and indicate that a presynaptic mechanism is involved in this inhibition.

INTRODUCTION The preceding paper 27 revealed that most neurones in the solitary tract nucleus have a single excitatory input, such as that from the larynx. This laryngeal input was found to be subject to inhibitory influences, particularly from neural activity carried in the superior laryngeal nerve (SLN), the glossopharyngeal nerve (IX), and the infraorbital nerve (IO). Afferent (and corticofugal) inhibition has also been reported in studies of other

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brain stem relay nuclei, including the dorsal column nuclei (for review, see Mountcastle and Darian-Smith 18) and the trigeminal sensory nuclei (for review, see DarianSmith 5, Dubner and Sessle 7,8, Sessle and Dubner29). Some of these investigations have indicated t h a t a presynaptic mechanism largely accounts for this effect. Moreover, axo-axonic synapses have been described11,12,14, 36 in these nuclei and probably constitute the morphological basis of this presynaptic inhibition. In view of these findings and the recent description3,22, 23 of presynaptic depolarization (PD) of SLN brain stem endings produced by cerebral cortical, vagal and aortic nerve conditioning stimulation, the present study was initiated to determine whether the inhibition observed in solitary tract neurones could be accounted for by similar presynaptic mechanisms. METHODS

Preparation of animals This study is based on experiments carried out in 15 adult cats (2.5-4,5 kg) anaesthetized with chloralose (60 mg/kg) and in two decerebrate cats. The preceding paper 27 has described the methods for preparation of the animals and for exposure of the caudal brain stem, the larynx, the pharyngeal branch of the vagus nerve (Phar X), the hypoglossal nerve (XII), and SLN, IX and IO. The nodose ganglion was also carefully exposed in this study and a plastic platform, which was firmly fixed to the stereotaxic apparatus, was placed beneath the ganglion to minimize movement and altow microelectrode recordings of ganglion neurones.

Recordingprocedures The animal was kept on its back and the activity olr single neurones in the ganglion~was recorded extracellularly with microelectrodes. It was usually necessary to remove part of the fibrous capsule that ensheathed the ganglion so that the microelectrodes could be inserted without damage to their tips. The recorded neuronal activity was amplified and displayed on an oscilloscope; photographic records were taken of selected responses.

Stimulation procedures As the micf6electrode was advanced in the ganglion, SLN was stimulated (0.01-5.0 mA, 0.1 msec) at 1/sec so that neurones innervating the larynx could be located. The excitatory receptive field of many of these neurones was investigated using a plastic probe. The conduction path from the SLN stimulating site to the ganglion recording site was measured so that the conduction velocity of single laryngeal neurones could be estimated. In addition to this orthodromic excitation of nodose ganglion neurones, antidr0mic activation was attempted. A pair of bipolar electrodes was located in the exposed brain stem 0-1 mm rostral to the obex. Localization in the vicinity of the solitary tract nucleus was achieved utilizing stereotaxic coordinates, direct visualization, :and recordings of the maximum evoked response to SLN stimulation. In 10

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animals a pair of bipolar electrodes was also placed in the contralateral nuclear region. Both ipsilateral and contralateral sites were subsequently verified histologically. The brain stem electrodes were used to stimulate (0.05-5.0 mA, 0.1 msec) the brain stem endings of single primary afferent neurones recorded in the ganglion. Antidromic activation of a neurone was based on a consistent, all-or-none response with short-latency to brain stem stimulation rates of 100/sec or more.

Conditioning procedures A presynaptic influence of cranial nerve activity on the brain stem endings of ganglion neurones was tested indirectly by determining the effect of preceding conditioning stimuli on the level of excitation of the axonal endings of single neurones antidromically activated from the brain stem. The technique for testing for an effect of conditioning was a modification of Wall's method a7 for determining excitability changes and similar to that described for single trigeminal primary4, s and corticofugal 7,8 afferent endings and for vagal primary afferent endings 3. An increase in excitability of the brain stem endings of a ganglion neurone produced by conditioning stimuli was reflected as an increase in the probability of occurrence of the neurone's antidromic response to the brain stem stimulus. This increase in excitability was a measure of PD which is indicative of presynaptic inhibitionlO,25; a decrease in excitability would reflect presynaptic hyperpolarization (PH). The time course of a conditioning effect was determined by comparing, at various conditioning-test intervals, the probability of occurrence of the neurone's antidromic response to 10 successive (1/sec) brain stem stimuli in the presence of a conditioning stimulus with its control probability to 10 brain stem test stimuli without any preceding conditioning stimulus. The conditioning stimuli were similar to those used ~7 for testing conditioning effects on the excitatory input of solitary tract neurones - - single bipolar electrical stimulation of SLN, IX, IO, Phar X and XII. No cerebral cortical conditioning stimulus was used, but the mechanical conditioning stimuli were applied to the upper lip, larynx and intraoral structures in addition to the canine teeth. RESULTS

Location and input A total of 106 single neurones were investigated in the nodose ganglion. The majority of these neurones had a laryngeal input, but the input to 22 neurones could not be satisfactorily demonstrated although many discharged in phase with respiration. These 22 neurones were generally distributed in the ganglion but the remaining 84 neurones with an identified laryngeal input were found near the entrance of SLN into the ganglion in a location similar to that described by Mei 15. No neurone recorded in the ganglion could be excited by stimulation of any of the exposed nerves other than SLN. However in more proximal parts of the ganglion, a field response with a 1-2 msec latency to XII stimulation was often observed, supporting the results of Zapata and Torrealba as which suggested that the ganglion may be a site for passage of XII afferents and perhaps a locale of their cell bodies.

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Receptive fieM and conduction velocity Neurones excited by SLN stimulation had small ipsilateral laryngeal mechanoreceptive fields (2-10 m m diameter) that were particularly concentrated on the dorsal surface overlying the arytenoid cartilage, thyroarytenoid muscle and aryepiglottic fold. A typical field is indicated in Fig. 3. No difference was noted between anaesthetized and decerebrate animals in the receptive field properties (or conditioning effects) of these neurones except for their responses to water applied to the receptive field. Water excited most laryngeal units tested in the decerebrate preparations but, in accordance with the observation of Storey 34, failed to activate more than 90 ~ of the neurones tested in anaesthetized animals. The conduction velocity of 77 of the laryngeal neurones was estimated from their latency to SLN stimulation and the conduction distance from the SLN stimulation site to the ganglion recording site. Over 90 ~o of the units had conduction velocities indicative of small myelinated (AO) nerve fibres (Fig. 1A). Only 3 of the units had conduction velocities greater than 35 m/sec and two conducted at less than 3.0 m/sec (suggesting unmyelinated nerve fibres).

Brain stem projection Fifty laryngeal units were tested to see if they projected to the region of the brain stem stimulating electrodes located in the ipsilateral solitary tract nucleus just rostral to the obex. A projection to this level of the nucleus was identified in 41 neurones on the basis of an antidromic response to stimulation at the brain stem site

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Fig. 2. Effects of conditioningstimuli applied to the superior laryngeal nerve (SLN), the glossopharyngeal nerve (IX), and the canine tooth on the excitability of a laryngeal neurone antidromically activated from the brain stem region of the solitary tract nucleus. An increase in excitability of the neurone's brain stem endings as a result of a conditioning stimulus was reflected as an increase in the probability of occurrence of the neurone's antidromic response. The time course of a conditioning effect was obtained by comparing, at various conditioning-test intervals, the control probability of occurrence of the antidromic response to 10 brain stem test stimuli (open circles) with the probability of occurrence of the response to a similar number of brain stem stimuli in the presence of a preceding conditioning stimulus. Actual records from this neurone are shown in the upper part of the figure. The left upper record illustrates the neurone's antidromic response to brain stem stimulation at 200/sec. The following 3 records in the upper row show 3 sequential responses of the neurone to a brain stem test stimulus. Only one antidromic response occurred in this control sequence, but when the brain stem stimulus was preceded at 40 msec by a mechanical conditioning stimulus applied to the canine, there was a marked increase in excitability of the neurone's brain stem endings. This is illustrated in the lower row where the neurone was antidromically activated by each brain stem stimulus. Negative polarity upwards; time calibration, 2.0 msec; voltage calibration, 0.1 mV. (Fig. 2). Thirty-five o f these n e u r o n e s had a n a n t i d r o m i c latency less t h a n 2.5 msec, a n d the d i s t r i b u t i o n o f latencies is shown in Fig. lB. A p r o j e c t i o n to the c o n t r a l a t e r a l b r a i n stem was tested in 16 o f the 41 neurones, a n d a n a n t i d r o m i c response to c o n t r a lateral b r a i n stem s t i m u l a t i o n was o b t a i n e d i n 10 o f them. T h e 22 n o n - l a r y n g e a l n e u r o n e s with a n unidentified i n p u t could also be antidromically activated f r o m the ipsilateral b r a i n stem. However, o f 11 that were tested to contralateral as well as to ipsilateral b r a i n stem s t i m u l a t i o n only two were f o u n d to project bilaterally.

Excitability changes T h e effects o f cranial nerve c o n d i t i o n i n g s t i m u l a t i o n o n the excitability o f the b r a i n stem endings were examined in the 41 laryngeal n e u r o n e s a n t i d r o m i c a l l y activated from the ipsilateral solitary tract nucleus. N o clear evidence o f a decrease in excitability (PH) was n o t e d in these units with a n y c o n d i t i o n i n g stimulus. However, a n increase in excitability or P D was d e m o n s t r a t e d in all b u t two n e u r o n e s as a result o f a c o n d i t i o n i n g stimulus applied to S L N or to the larynx. This P D effect typically

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Fig. 3. Effects of conditioning stimuli on the excitability of a laryngeal neurone antidromically activated from the ipsilateral and contralateral brain stem. Excitability changes and their time courses were measured as described for Fig. 2. Effective conditioning stimuli were those applied to the superior laryngeal nerve (SLN), the glossopharyngeal nerve (IX), the canine tooth, and the hypoglossal nerve (XII). The time courses of the effects on the neurone's contralateral brain stem endings are shown in A, and B illustrates the time courses of effects on its endings in the ipsilateral solitary tract nucleus. The laryngeal mechanoreceptive field of the neurone is indicated (arrow) by the black patch on the illustration of the exposed larynx.

s t a r t e d a b o u t 10 msec after the c o n d i t i o n i n g stimulus was given, r e a c h e d its p e a k b y 20-40 msec, a n d lasted for 300 msec (Figs. 2 a n d 3). I n some n e u r o n e s the P D was still o b v i o u s as long as 600 msec after the c o n d i t i o n i n g stimulus was given. C o n d i t i o n i n g stimuli a p p l i e d to I X a n d to IO o r o t h e r structures i n n e r v a t e d by the trigeminal nerve were also effective in eliciting P D in the b r a i n stem endings o f laryngeal units. H o w e v e r , P D was n o t as c o m m o n as that occurring with l a r y n g e a l c o n d i t i o n i n g stimulation : I X c o n d i t i o n i n g s t i m u l a t i o n p r o d u c e d P D in 24 o f 32 laryngeal neurones tested a n d trigeminal c o n d i t i o n i n g stimuli resulted in P D in 28 o f 34 units (Figs. 2 a n d 3). P D could be p r o d u c e d by IO c o n d i t i o n i n g stimuli or by mechanical c o n d i t i o n i n g stimulation o f the u p p e r lip a n d especially the teeth such as the canine. It was usually s h o r t e r in d u r a t i o n t h a n t h a t p r o d u c e d by S L N o r I X c o n d i t i o n i n g stimuli a n d typically lasted for a b o u t 120 msec (Fig. 3). Very few o f the laryngeal n e u r o n e s showed an increase in excitability o f their

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brain stem endings with XII or Phar X conditioning stimulation. XII conditioning effects (e.g. Fig. 3) occurred in only 3 of 32 neurones tested, and 7 of 31 neurones exhibited PD with Phar X conditioning. PD could also be demonstrated in the contralateral brain stem endings of the 10 laryngeal afferent units terminating bilaterally in the brain stem. SLN, IX and sometimes IO or tooth conditioning were effective in producing PD contralaterally. However, the increase in excitability with SLN and IX conditioning was shorter in duration than that occurring on the ipsilateral endings. This is illustrated in Fig. 3 which shows the time courses of PD occurring in the ipsilateral and contralateral brain stem endings of a laryngeal neurone. PD was not restricted solely to laryngeal afferent neurones. Excitability changes were also tested in the 22 neurones with an unidentified input. SLN conditioning stimuli could produce PD in the brain stem endings of 19 of these units, and IX was an effective stimulus in 8 of 15 neurones tested. No change in excitability could be demonstrated with any of the other conditioning stimuli used in this study. DISCUSSION

The laryngeal information carried into the brain stem by SLN afferents is concerned with the initiation of both complex (e.g. swallowing) and 'elementary '6 reflex activities (for review, see Dory 6, and Storey 3~) and with conscious sensation from the larynx 2,19,20. The laryngeal units studied in the present investigation were probably involved in both these functions. Their receptive field properties, stimulation threshold, conduction velocities, and discharge characteristics were similar to those described by other workersl,9,15-17,24,zt, za for laryngeal afferents that are capable of initiating swallowing and possibly the elementary reflexes33,zS. In addition to a demonstrated projection to the ipsilateral solitary tract nucleus, many laryngeal units could also be antidromically activated from the contralateral brain stem. A bilateral projection of vagal nerve afferents to the caudalmost part of the solitary tract nucleus as well as the commissural nucleus of Cajal has been described in both anatomical 13 and electrophysiologica121 investigations in cat. However, Sessle 27 failed to find any neurones in the solitary tract nucleus that could be excited by contralateral SLN stimulation, although some neurones in the adjacent reticular formation were activated. These findings would suggest that laryngeal afferents, unlike vagal afferents, do not terminate in the contralateral solitary tract nucleus proper but may end in the reticular formation or the commissural nucleus. The contralateral antidromic responses recorded in the present study could be accounted for by the contralateral brain stem stimulation activating endings in either of these latter two regions. A decrease in excitability in these laryngeal afferent endings could not be produced by any of the conditioning stimuli used. This would suggest that PH, which has recently been described on some primary afferent and corticofugal endings in the trigeminal brain stem sensory nuclei 2s, has no regulatory role in the solitary tract nucleus, at least for neurones with a laryngeal input. Support for this view comes

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from the failure 27 to find any evidence of facilitatory conditioning effects in solitary tract neurones activated by laryngeal stimulation. However, some neurones in this nucleus with a IX input could be facilitated for a period of time suggestive of a presynaptic mechanism. The possibility that IX primary afferent units are subject to PH, as well as to PD, is presently being investigated in this laboratory. The relative effectiveness of the various conditioning stimuli in producing PD is similar to that noted 27 in their inhibitory effects on solitary tract neurones. This finding, together with the close correlation in the onset, peak and time course between PD of laryngeal units and inhibition of solitary tract neurones, indicate that a presynaptic mechanism largely accounts for the inhibitory influences in the solitary tract nucleus. PD can also be demonstrated in SLN endings using conditioning stimulation of the cerebral cortex and vagal and aortic nervesa,Ze, 2a. Although he gave no details, Rudomin 22 did mention that PD of SLN endings could also be produced by trigeminal nerve conditioning stimuli. This adds support to the present findings of a considerable presynaptic influence from orofacial areas on the laryngeal input to the central nervous system. The possible significance of this regulatory role of the trigeminal region has been discussed elsewhere 3°. Nevertheless, reference should also be made to the study of Seizer and Spencer z8 who noted PD of spinal visceral afferents produced by somatic nerve conditioning stimulation and implicated this as a possible factor contributing to mechanisms of visceral and referred pain. The present findings of an orofacial presynaptic influence on laryngeal afferent endings also constitutes a somatic-visceral interaction and may have similar implications. PD was not however restricted to SLN endings in the brain stem. An increase in excitability could also be produced with SLN and IX conditioning stimuli in the brain stem endings of non-laryngeal units. The receptive fields of these neurones could not be determined but it seems likely that many of them innervated lower cervical and thoracic visceral structures since the cell bodies of neurones supplying pulmonary and cardiac areas in particular are interspersed with laryngeal neurones in the ganglion 15. Moreover, many of the units were found to discharge in phase with respiration. Barillot a has also observed that SLN conditioning stimulation may produce PD of myelinated vagal afferents innervating oesophageal, pulmonary and cardiac areas. Such laryngeal regulation may be of functional significance in the organization of the elementary and more complex reflexes with which the larynx is concerned~,a z. ACKNOWLEDGEMENTS

The technical assistance of Mr. M. Kalovsky, Mrs. M. McKenzie and Miss B. Holmwood is gratefully acknowledged. I also express my thanks to Dr. Arthur Storey for his advice and aid in some of the experiments and for critically reviewing the manuscript, and to Dr. Ronald Dubner for his constructive comments on the manuscript. The study was supported by Grant D.G. 73 from the Canadian Medical Research Council.

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