The Journal of Neurophysiology Vol. 78 No. 4 October 1997, pp. 2186-2192
Copyright ©1997 The American Physiological Society

Excitatory and Inhibitory Inputs From Saccular Afferents to Single Vestibular Neurons in the Cat

Y. Uchino, H. Sato, and H. Suwa

Department of Physiology, Tokyo Medical College, Shinjuku-ku, Tokyo 160, Japan

Uchino, Y., H. Sato, and H. Suwa. Excitatory and inhibitory inputs from saccular afferents to single vestibular neurons in the cat. J. Neurophysiol. 78: 2186-2192, 1997. Connections from saccular afferents to vestibular neurons were studied by means of intracellular recordings of excitatory (E) and inhibitory (I) postsynaptic potentials (PSPs) in vestibular neurons after focal stimulation of the saccular macula in decerebrated cats. Focal stimulation was given to the saccular macula in two ways, in which the polarity of stimulus current via a pair of electrodes was changed. In group A, one of the electrodes was inserted into the ventral and the other into the dorsal edge of the saccular macula. The focal stimulation was across the striola so that the reversal of morphological polarization in hair cells was bridged by the pulse stimulus. In 22/36 vestibular neurons tested, the stimulation of the saccular macula evoked monosynaptic (1.2 ms) EPSPs, including EPSP-IPSP sequences, with one polarity of stimulation, and disynaptic (1.5 ms) IPSPs when the polarity of the stimulus current was changed. In 14/36 neurons, the response pattern was the same regardless of the stimulus polarity; EPSPs (12/36) or IPSPs (2/36). In group B, a pair of electrodes was inserted into the dorsal edge of the saccular macula, so that the striola was not bridged by the current stimulus. In all of the vestibular neurons tested, the response pattern was always the same regardless of the polarity: mono- (22/31) and disynaptic (3/31) EPSPs or disynaptic IPSPs (6/31). In addition, the saccular nerve was stimulated after removing the macula in some cats (group C). The stimulation of the saccular nerve evoked EPSPs in 62 vestibular neurons (including EPSP-IPSP sequences in 31 neurons) and IPSPs in 19 vestibular neurons. Convergence between the saccular nerve and other vestibular nerves was studied by the intracellular recording of PSPs. Fifty-six percent (18/32) of the saccular-activated neurons had excitatory and/or inhibitory potentials evoked after stimulation of the utricular nerve and the horizontal and anterior semicircular canal nerves, and 44% (19/43) of the neurons received inputs from the posterior semicircular canal nerve. The results support the hypothesis that saccular afferents from one population of hair cells activate vestibular neurons monosynaptically and that afferents from another population of hair cells located on the opposite side of the striola appear to project to the same vestibular neurons disynaptically via inhibitory interneurons. Neural circuits from saccular afferents to vestibular neurons, which we term cross-striolar inhibition, thus may provide a mechanism for increasing the sensitivity to vertical linear acceleration. The circuit described is provided not only with high sensitivity but also with input noise-resistant characteristics.

This article has been cited by other articles:

				F. Deriu, E. Ortu, S. Capobianco, E. Giaconi, F. Melis, E. Aiello, J. C. Rothwell, and E. Tolu Origin of sound-evoked EMG responses in human masseter muscles J. Physiol., April 1, 2007; 580(1): 195 - 209. [Abstract] [Full Text] [PDF]

				J.-r. Tian, E. Mokuno, and J. L. Demer Vestibulo-Ocular Reflex to Transient Surge Translation: Complex Geometric Response Ablated by Normal Aging J Neurophysiol, April 1, 2006; 95(4): 2042 - 2054. [Abstract] [Full Text] [PDF]

				F. Deriu, E. Tolu, and J. C. Rothwell A Sound-Evoked Vestibulomasseteric Reflex in Healthy Humans J Neurophysiol, May 1, 2005; 93(5): 2739 - 2751. [Abstract] [Full Text] [PDF]

				D. E. Angelaki Eyes on Target: What Neurons Must do for the Vestibuloocular Reflex During Linear Motion J Neurophysiol, July 1, 2004; 92(1): 20 - 35. [Abstract] [Full Text] [PDF]

				M. Zakir, D. Huss, and J. D. Dickman Afferent Innervation Patterns of the Saccule in Pigeons J Neurophysiol, January 1, 2003; 89(1): 534 - 550. [Abstract] [Full Text] [PDF]

				K. Kushiro, M. Dai, M. Kunin, S. B. Yakushin, B. Cohen, and T. Raphan Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys J Neurophysiol, November 1, 2002; 88(5): 2445 - 2462. [Abstract] [Full Text] [PDF]

				D. E. Angelaki, S. D. Newlands, and J. D. Dickman Primate Translational Vestibuloocular Reflexes. IV. Changes After Unilateral Labyrinthectomy J Neurophysiol, May 1, 2000; 83(5): 3005 - 3018. [Abstract] [Full Text] [PDF]

				J. A. BUTTNER-ENNEVERA A Review of Otolith Pathways to Brainstem and Cerebellum Ann. N.Y. Acad. Sci., May 28, 1999; 871(1): 51 - 64. [Abstract] [Full Text] [PDF]

				Y. UCHINO, H. SATO, K. KUSHIRO, M. ZAKIR, M. IMAGAWA, Y. OGAWA, M. KATSUTA, and N. ISU Cross-Striolar and Commissural Inhibition in the Otolith System Ann. N.Y. Acad. Sci., May 28, 1999; 871(1): 162 - 172. [Abstract] [Full Text] [PDF]

				D. E. Angelaki Three-Dimensional Organization of Otolith-Ocular Reflexes in Rhesus Monkeys. III. Responses to Translation J Neurophysiol, August 1, 1998; 80(2): 680 - 695. [Abstract] [Full Text] [PDF]