Summary
1.The somatic location and axonal projections of inhibitory vestibular nucleus neurons activated by the horizontal semicircular canal nerve (HCN) were studied in anesthetized cats. Cats were anesthetized with ketamine hydrochloride and pentobarbital sodium. 2.Intracellular recordings were obtained from 11 neck extensor motoneurons which were identified by antidromic activation from the dosai rami (DR) in the C1 segment. Stimulation of the ipsilateral (i-) HCN and the ipsilateral abducens (AB) nucleus evoked IPSPs in the motoneurons. These IPSPs were fully or partially occluded when they were evoked simultaneously. 3. Intracellular recordings were obtained from 8 AB motoneurons. Stimulation of the i-HCN and the i-C1DR motoneuron pool evoked IPSPs in the AB motoneurons. These IPSPs were also partially occluded when they were evoked simultaneously, which implied that some HCN-activated neurons inhibit both i-AB motoneurons and ipsilateral neck motoneurons. 4. Unit activity was extracellularly recorded from 30 vestibular neurons that were activated monosynaptically by i-HCN stimulation. Their axonal projections were determined by stimulating the i-AB nucleus and the i-C1DR motoneuron pool. Eight neurons were activated by both stimuli, and were termed vestibulooculo-collic (VOC) neurons. Their axonal branching was examined by means of local stimulation in and around the i-AB nucleus and the i-C1DR motoneuron pool. Eighteen neurons were antidromically activated from the i-C1DR motoneuron pool but not from the i-AB nucleus. These were termed vestibulo-collic (VC) neurons. Four neurons were activated from the i-AB nucleus but not from the ventral funiculus in the C1 segment, and were termed vestibulo-ocular (VO) neurons. The HCN-activated inhibitory neurons were mostly localized in the rostroventral part of the medial vestibular nucleus. 5. Horseradish peroxidase (HRP) was injected iontophoretically into descending axons of 2 HCN-activated inhibitory VOC neurons which were identified by stimulation of the i-HCN and the i-AB nucleus. Axon collaterals were ramified from a stem axon in the ventral funiculus, and entered the gray matter and spread in the laminae VIII and IX. Terminal boutons were distributed over the medial and the ventromedial parts of the vental horn in the C1 segment.
Similar content being viewed by others
References
Baker RG, Mano N, Shimazu H (1969) Postsynaptic potentials in abducens motoneurons induced vestibular stimulation. Brain Res 15:577–580
Carpenter M, Cowie R (1985) Connections and oculomotor projections of the superior vestibular nucleus and cell group “y”. Brain Res 336:265–287
Cohen B, Suzuki JI, Bender MB (1964) Eye movements from semicircular canal nerve stimulation in the cat. Ann Otol (St. Louis) 73:153–170
Fukushima K, Peterson BW, Wilson VJ (1979) Vestibulospinal reticulospinal and interstitiospinal pathways in the cat. In: Granit R, Pompeiano O (eds) Reflex contral of posture and movements. Prog Brain Res Vol 50. Elsevier, Amsterdam, pp 121–136
Geyer SW, Gudden W, Betz H, Gnahn H, Weindl A (1987) Colocalozation of choline acetyltransferase and postsynaptic glycine receptors in motoneurons of rat spinal cord demonstrated by immunocytochemistry. Neurosci Lett 82:11–15
Graf W, Ezure K (1986) Morphology of vertical canal related second order vestibular neurons in the cat. Exp Brain Res 63:35–48
Highstein SM (1973) Synaptic linkage in the vestibuloocular and cerebellovestibular pathways to the VIth nucleus in the rabbit. Exp Brain Res 17:301–314
Hirai N, Uchino Y (1984) Floccular influence on excitatory relay neurones of vestibular reflexes of anterior semicircular canal origin in the cat. Neurosci Res 1:327–340
Hongo T, Kudo N, Sasaki S, Yamashita M, Yoshida K, Ishizuka N, Mannen H (1987) Trajectory of group Ia and Ib fibers from the hind-limb muscles at the L3 and L4 segments of the spinal cord of the cat. J Comp Neurol 262:159–194
Ishizuka N, Mannen H, Sasaki S-I, Shimazu H (1980) Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system. Neurosci Lett 16:143–148
Isu N, Sakuma A, Hiranuma K, Ichikawa T, Uchino Y (1990)Localization and synaptic effects of inhibitory vestibulocollic neurons activated by the posterior semicircular canal nerve in cats. Neurosci Lett 119:163–166
Isu N, Uchino Y, Nakashima H, Satoh S, Ichikawa T, Watanabe S (1988) Axonal trajectories of posterior canal-activated secondary vestibular neurons and their coactivation of extraocular and neck flexor motoneurons in the cat. Exp Brain Res 70:181–191
Isu N, Yokota J (1983) Morphophysiological study on the divergent projection of axon collaterals of medial vestibular nucleus neurons in the cat. Exp Brain Res 53:151–162
Iwamoto Y, Kitama T, Yoshida K (1990a) Vertical eye movement-related secondary vestibular neurons ascending in the medial longitudinal fasciculus in the cat. I. Firing properties and projection pathways. J Neurophysiol 63:902–917
Iwamoto Y, Kitama T, Yoshida K (1990b) Vertical eye movement-related secondary vestibular neurons ascending in the medial longitudinal fasciculus in the cat. II. Direct connections with extraocular motoneurons. J Neurophysiol 63:918–935
Mano N, Oshima T, Shimazu H (1968) Inhibitory commissural fibers interconnecting the bilateral vestibular nuclei. Brain Res 8:378–382
McCrea RA, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264:547–570
McCrea RA, Yoshida K, Berthoz A, Baker R (1980) Eye movement related activity and morphology of second order vestibular neurons terminating in the cat abducens nucleus. Exp Brain Res 40:468–473
McCrea RA, Yoshida K, Evinger C, Berthoz A (1981) The location, axonal arborization, and termination sites of eye-movement-related secondary vestibular neurons demonstrated by intraaxonal HRP injection in the alert cat. In: Fuchs A, Becker W (eds) Progress in oculomotor Research. Developments in neuroscience, Vol 12. Elsevier, Amsterdam, pp 379–386
Ohgaki T, Curthoys IS, Markham CH (1988) Morphology of physiologically identified second-order vestibular neurons in cat, with interacellulary injected HRP. J Comp Neurol 276:387–411
Rapoport S (1978) Location of sternocleidomastoid and trapezius motoneurons in the cat. Brain Res 156:339–344
Richmond FJR, Scott DA, Abrahams VC (1978) Distribution of motoneurons to the neck muscles, biventer cervicis, splenius and complexus in the cat. J Comp Neurol 181:451–464
Shimazu H (1983) Neuronal organization of the premotor system controlling horizontal conjugate eye movements and vestibular nystagmus. In: Desmedt JE (eds) Motor control mechanisms in health and disease. Raven Press, New York, pp 565–588
Shimazu H, Precht W (1965) Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J Neurophysiol 28:991–1013
Shinoda Y, Ohgaki T, Futami T, Sugiuchi Y (1988) Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons. In: Pomperiano O, Allum J (eds) Vestibulospinal contral of postare and locomotion. Prog Brain Res, Vol 76. Elsevier, Amsterdam, pp 17–27
Spencer RF, Wenthold RJ, Baker R (1989) Evidence for Glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus. J Neuroscience 9:2718–2736
Stillhard G (1981) Musculi longus capitis et splenius der ratte und innervierende motoneurone. Acta Neuropathol 53:267–274
Triller A, Cluzeaud F, Pfeiffer F, Betz H, Korn H (1985) Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J Cell Biol 101:683–688
Uchino Y, Hirai N (1984) Axon collaterals of anterior semicircular canal-activated vestibular neurons and their coactivation of extraocular and neck motoneurons in the cat. Neurosci Res 1:309–325
Uchino Y, Hirai N, Suzuki S, Watanabe S (1981) Properties of secondary vestibular neurons fired by stimulation of ampullary nerve of the vertical, anterior or posterior, semicircular canals in the cat. Brain Res 223:273–286
Uchino Y, Isu N (1990/91) Properties of vestibulo-ocular and/or vestibulo-collic neurons in the cat. In: Berthoz A, Graf W, Vidal PP (eds) The head-neck sensorymotor system, Vol 82. Oxford University Press, New York Oxford, pp 14–24
Uchino Y, Isu N, Ichikawa T, Satoh S, Watanabe S (1988) Properties and localization of the anterior semicircular canal-activated vestibulocollic neurons in the cat. Exp Brain Res 71:345–352
Uchino Y, Isu N, Sakuma A, Ichikawa T, Hiranuma K (1990a)Axonal trajectories of inhibitory vestibulocollic neurons activated by the anterior semicircular canal nerve and their synaptic effects on neck motoneurons in the cat. Exp Brain Res 82:14–24
Uchino Y, Sasaki S-I, Imagawa M, Uchino H, Isu N, Sakuma A (1990b) Properties and axonal trajectories of inhibitory vestibulocollic neurons in the horizontal canal system of the cat. Neurosci Res Suppl 11:S139
Uchino Y, Suzuki S (1983) Axon collaterals to the extraocular motoneuron pools of inhibitory vestibuloocular neurons activated from the anterior, posterior and horizontal semicircular canals in the cat. Neurosci Lett 37:129–135
Uchino Y, Suzuki S, Miyazawa T, Watanabe S (1979) Horizontal canal input to cat extraocular motoneurons. Brain Res 177:231–240
Van den Pol AN, Gorcs T (1988) Glycine and glycine receptor immunoreactivity in brain and spinal cord. J Neurosci 8:472–492
Vidal PP, Corvisier J, Berthoz A (1983) Eye and neck motor signals in periabducens reticular neurons of the alert cat. Exp Brain Res 53:16–28
Wilson VJ, Maeda M (1974) Connections between semicircular canals and neck motoneurons in the cat. J Neurophysiol 37:346–357
Wilson VJ, Precht W, Dieringer N (1983) Responses of different compartments of cat's splenius muscle to optokinetic stimulation. Exp Brain Res 50:153–156
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Isu, N., Sakuma, A., Hiranuma, K. et al. The neuronal organization of horizontal semicircular canalactivated inhibitory vestibulocollic neurons in the cat. Exp Brain Res 86, 9–17 (1991). https://doi.org/10.1007/BF00231035
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00231035