Journal of Neurophysiology, Vol 70, Issue 6 2425-2441, Copyright © 1993 by APS

ARTICLES

Sensorimotor transformation in the cat's vestibuloocular reflex system. I. Neuronal signals coding spatial coordination of compensatory eye movements

W. Graf, J. Baker and B. W. Peterson
Rockefeller University, New York 10021.

1. Coordinate transformation between vestibular and oculomotor reference frames is required to produce compensatory, vestibuloocular reflex (VOR) eye movements in view of the differing, although similar, peripheral three-dimensional geometry of the semicircular canals and the extraocular muscles. This transformation requires convergence of canal-specific signals at some level in the VOR arc. 2. To investigate the networks that underlie the transformation between oculomotor and vestibular reference frames for spatial coordination of compensatory eye movements, we recorded intracellularly in decerebrate cats from 93 identified second-order vestibulooculomotor and abducens internuclear neurons in the medial longitudinal fasciculus (MLF) between abducens and trochlear nuclei and characterized their spatial response properties. Neurons were classified according to whether they were activated from the labyrinth ipsi- or contralateral to the recording site and according to the canal from which they received their strongest input. Our data revealed neurons that carried single- and multiple-canal signals. 3. Twenty-two neurons received their primary input from the ipsi- or contralateral anterior canal (AC). Ten nonconvergent AC neurons responded maximally to rotation in a plane within 10 degrees of the AC plane, whereas 6 AC neurons received sufficient convergent input from the orthogonal vertical canals to shift their plane of maximum response > 10 degrees from the AC plane. Of 29 ipsi- and contralateral posterior canal (PC) neurons, 9 were non-convergent, whereas 13 received sufficient convergent input from the orthogonal vertical canals to shift their response plane > 10 degrees from the PC plane. The rotational responses of 6 AC and 12 PC neurons indicated that they received convergent input from the horizontal canals. However, when these responses were averaged, the horizontal responses tended to cancel, leaving little net population response to horizontal rotation. We also encountered 19 ascending axons of second-order neurons activated primarily from the horizontal canals. Nine of these received significant input from the vertical canals, but the mean population response was within 4 degrees of the horizontal canal plane. 4. Our results demonstrate single canal responses and specific canal-canal convergence within the population of vertical vestibulooculomotor neurons. This convergence is thought to participate in the coordinate transformation within the specific geometry of the VOR system. The data indicate response shifts of a population of AC neurons toward the plane of the inferior oblique muscle, and of a population of PC neurons toward the plane of the superior oblique muscle. Conspicuously absent are neurons that fall into the plane of either the superior rectus or the inferior rectus muscles. (ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				Y. Xiang, S. B. Yakushin, B. Cohen, and T. Raphan Modeling Gravity-Dependent Plasticity of the Angular Vestibuloocular Reflex With a Physiologically Based Neural Network J Neurophysiol, December 1, 2006; 96(6): 3349 - 3361. [Abstract] [Full Text] [PDF]

				S. B. Yakushin, T. Raphan, and B. Cohen Spatial Properties of Central Vestibular Neurons J Neurophysiol, January 1, 2006; 95(1): 464 - 478. [Abstract] [Full Text] [PDF]

				S. B. Yakushin, T. Raphan, J. A. Buttner-Ennever, J.-I. Suzuki, and B. Cohen Spatial Properties of Central Vestibular Neurons of Monkeys After Bilateral Lateral Canal Nerve Section J Neurophysiol, December 1, 2005; 94(6): 3860 - 3871. [Abstract] [Full Text] [PDF]

				A. M. Green and D. E. Angelaki An Integrative Neural Network for Detecting Inertial Motion and Head Orientation J Neurophysiol, August 1, 2004; 92(2): 905 - 925. [Abstract] [Full Text] [PDF]

				C. D. Balaban, D. M. McGee, J. Zhou, and C. A. Scudder Responses of Primate Caudal Parabrachial Nucleus and Kolliker-Fuse Nucleus Neurons to Whole Body Rotation J Neurophysiol, December 1, 2002; 88(6): 3175 - 3193. [Abstract] [Full Text] [PDF]

				J. D. Dickman and D. E. Angelaki Vestibular Convergence Patterns in Vestibular Nuclei Neurons of Alert Primates J Neurophysiol, December 1, 2002; 88(6): 3518 - 3533. [Abstract] [Full Text] [PDF]

				H. Straka, S. Holler, and F. Goto Patterns of Canal and Otolith Afferent Input Convergence in Frog Second-Order Vestibular Neurons J Neurophysiol, November 1, 2002; 88(5): 2287 - 2301. [Abstract] [Full Text] [PDF]

				M. Rohregger and N. Dieringer Principles of Linear and Angular Vestibuloocular Reflex Organization in the Frog J Neurophysiol, January 1, 2002; 87(1): 385 - 398. [Abstract] [Full Text] [PDF]

				D. E. Angelaki and J. D. Dickman Spatiotemporal Processing of Linear Acceleration: Primary Afferent and Central Vestibular Neuron Responses J Neurophysiol, October 1, 2000; 84(4): 2113 - 2132. [Abstract] [Full Text] [PDF]

				S. I. Perlmutter, Y. Iwamoto, J. F. Baker, and B. W. Peterson Spatial Alignment of Rotational and Static Tilt Responses of Vestibulospinal Neurons in the Cat J Neurophysiol, August 1, 1999; 82(2): 855 - 862. [Abstract] [Full Text] [PDF]

				C. Siebold, J. F. Kleine, L. Glonti, T. Tchelidze, and U. Buttner Fastigial Nucleus Activity During Different Frequencies and Orientations of Vertical Vestibular Stimulation in the Monkey J Neurophysiol, July 1, 1999; 82(1): 34 - 41. [Abstract] [Full Text] [PDF]

				K. Zhang and T. J. Sejnowski A Theory of Geometric Constraints on Neural Activity for Natural Three-Dimensional Movement J. Neurosci., April 15, 1999; 19(8): 3122 - 3145. [Abstract] [Full Text] [PDF]

				H. Straka, S. Biesdorf, and N. Dieringer Canal-Specific Excitation and Inhibition of Frog Second-Order Vestibular Neurons J Neurophysiol, September 1, 1997; 78(3): 1363 - 1372. [Abstract] [Full Text] [PDF]

				Y. Uchino, H. Sato, M. Sasaki, M. Imagawa, H. Ikegami, N. Isu, and W. Graf Sacculocollic Reflex Arcs in Cats J Neurophysiol, June 1, 1997; 77(6): 3003 - 3012. [Abstract] [Full Text] [PDF]