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

1. Coordinate transformation between vestibular and oculomotor reference frames is required to produce compensatory, vestibuloocular reflex (VOR) eye movements in view of the differring, 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° 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° 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° 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° 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. We interpret our data such that a two-tier coordinate transformation takes place in the spatial domain of the vertical VORs. One part of the convergence occurs at the level of the vestibular nuclei by polysynaptic intrinsic pathways (for superior and inferior obliques), providing a functional transformation. The second necessary step is brought about by axon collaterals of second-order vestibular neurons within the oculomotor nucleus (for superior and inferior recti), providing a structural transformation. 5. Our hypothetical innervation scheme for sensorimotor transformation of vertical VORs is in accordance with the relevant data from the literature and with our own preliminary structure-function results.