Brain Research, 582 (1992) 147-153 © 1992 Elsevier Science Publishers B.V. All rights reserved. 0006-8993/92/$05.00

147

BRES 25203

Phasic modulation of transmission from vestibular inputs to reticulospinal neurons during fictive locomotion in lampreys Nathalie Bussi6res and R6jean Dubuc D~partement de Kinanthropologie, Universit~ du Quebec ?~Montreal, Montreal, Que. (Canada) and Centre de Recherche en Sciences Neurologiques, Universit~ de Montreal, Montreal, Que. (Canada)

(Accepted 18 February 1992) Key words: Locomotion; Vestibular input; Sensory modulation; Reticulospinal neuron; Brainstem; Lamprey

The aim of this study was to determine whether the transmission from sensory inputs to reticulospinal neurons is modulated during fictive locomotion in lampreys. Reticulospinal neurons play a key role in the control of locomotion; modulation of sensory transmission to these neurons might be of importance for the adaptation of the control they exert during locomotion. In this series of experiments, intracellular synaptic responses of reticulospinal neurons of the posterior rhombencephalic reticular nucleus elicited by electrical stimulation of vestibular nerves on each side were studied during fictive locomotion induced by 50/~M N-methyl-o-aspartate (NMDA). Interestingly, shortly after NMDA had reached the bath and much before locomotor discharges were apparent in the recorded ventral roots, there was a significant depression of the synaptic transmission from vestibular nerves. The effect was reversed by washing out the NMDA and persisted in the isolated brainstem after spinal transection at the first segmental level. As locomotor discharges appeared in the ventral roots, synaptic responses elicited by vestibular nerve stimulation showed a clear phasic modulation of their amplitude during the locomotor cycle. Responses to stimulation of the ipsilateral vestibular nerve were smaller during the ipsilateral burst discharge than during the contralateral activity, whilst responses to stimulation of the contralateral vestibular nerve were minimal during contralateral activity and maximal during ipsilateral activity. This opposite pattern of modulation observed in the same reticulospinal neuron suggests that the phasic modulation of vestibular transmission is not due to changes in the membrane properties of the reticulospinal cell but is produced at a pre-reticular level. Although the exact site of modulation in this disynaptic pathway has not yet been established, presynaptic mechanisms are possibly important. As in o t h e r vertebrates, the basic l o c o m o t o r p a t t e r n of lampreys is g e n e r a t e d by neuronal networks in the spinal cord (for review see ref. 13). These spinal locom o t o r networks have b e e n intensively studied in the last decade and a m o d e l of the spinal circuitry for segmental generation of locomotion has been p r o p o s e d based on the established synaptic connectivity of interneurons and m o t o n e u r o n s 4. Supraspinal structures have been shown to play a key role in the initiation and control of locom o t i o n 2'17A8. Two major descending systems are known to be involved: the reticulospinal and the vestibulospinal tracts 2°'21. Reticulospinal axons project along the entire rostro-caudal extent of the spinal cord 22 where they m a k e synaptic contacts with m o t o n e u r o n s and spinal interneurons involved in the generation of locomotion 3. It is likely that to exert an efficient control during locomotion, reticulospinal neurons require f e e d b a c k information from the spinal l o c o m o t o r networks as well as from sensory inputs. Reticulospinal neurons are rhythmically active during fictive l o c o m o t i o n 14'~5 and it has recently been shown 1° that this m o d u l a t i o n originates at least partly from the spinal cord, suggesting that the spinal l o c o m o t o r networks provide such a f e e d b a c k to the re-

ticulospinal neurons. M o r e o v e r , reticulospinal neurons receive sensory inputs from dorsal roots and dorsal columns 9 as well as from vestibular and trigeminal nerves n ' 12,21 This study was a i m e d at characterizing the influence of the l o c o m o t o r networks on the transmission of sensory inputs to reticulospinal neurons. Phasic modulation of transmission from sensory inputs has been well d o c u m e n t e d in the spinal cord of other vertebrates t'23. R e c e n t experiments in cats have shown that such modulation possibly occurs with respect to brainstem neurons 8. The present study was u n d e r t a k e n to d e t e r m i n e if a phasic m o d u l a t i o n of synaptic transmission occurs in reticulospinal neurons of lampreys during fictive locomotion and if so, to study eventually the cellular mechanisms involved. O u r study was concerned with the transmission to reticulospinal neurons in the posterior rhombencephalic reticular nucleus ( P R R N ) , which show rhythmic fluctuations of potential well correlated with ventral r o o t discharges in the rostral spinal cord. The transmission of disynaptic 21 vestibular inputs to these cells was studied during fictive locomotion. The majority of reticulospinal cells r e s p o n d to natural rotation 19 and therefore a m o d u l a t i o n of vestibular transmission to

Correspondence: R. Dubuc, D6partement de Kinanthropologie, Universit6 du Qu6bec ~ Montr6al, C.P.8888 succ. A, Montreal, Que. H3C 3P8, Fax: (1) (514) 343-2111.

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Fig. 1. A: schematic representation of the stimulation and recording paradigms (see text; i, ipsilateral; co, contralateral; VR, ventral root; Vest, vestibular; n, nerve; RS, reticulospinal). B: effects of NMDA (50 ~M) on synaptic responses elicited in a reticulospinal cell by stimulation of the ipsilateral (35/~A) and contralateral (45 pA) vestibular nerves. The amplitude of both responses were significantly reduced after NMDA. C: synaptic responses induced in another reticulospinal neuron by stimulation of the ipsilateral vestibular nerve in the isolated brainstem after a complete spinal transection of the first spinal segment (see 'Transection' in Fig. 1A). NMDA (50 pM) was applied twice (lst and 2nd NMDA) and complete recovery of the synaptic responses occurred each time.

b r a i n s t e m n e u r o n s will h a v e i m p o r t a n t c o n s e q u e n c e s o n the adaptation of the control they exert during locomo-

tion. Nine adult lampreys

(Ichthyomyzon unicuspis) 2 5 - 3 0

Fig. 2. A: phasic modulation of synaptic responses induced in a reticulospinal cell (membrane potential: -70 mV) by stimulation of the ipsilateral vestibular nerve (i Vest; 40/~A) during fictive locomotion. AI: the upper trace shows the intracellularly recorded membrane potential of the reticulospinal (RS) cell, while the two traces underneath represent the activity of the 4th ipsilateral (i) and 6th contralateral (co) ventral roots (VR). Note that the synaptic responses (top trace) evoked by stimulating the ipsilateral vestibular nerve during ipsilateral ventral root activity (arrows) are smaller than those evoked during the opposite phase. Az: averaged (top; n = 8) and superimposed (bottom; n = 4) synaptic responses induced during the ipsilateral and contralateral ventral root discharges. The dotted line on top of the averages represents the standard deviation. B: phasic modulation of synaptic responses of the same reticulospinal cell to contralateral vestibular stimulation (co Vest; 35/~A). The arrows point at synaptic responses which are smaller during the contralateral burst. B1,Bz:same as in A 1 and A 2 but synaptic responses were elicited by contralateral vestibular nerve stimulation.

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