Directional sensitivity of anterior, posterior, and horizontal canal vestibulo-ocular neurons in the cat

Neurons subserving the vestibulo-ocular reflex transform the directionality and timing of input from semicircular canals into commands that are approp riate to rotate the eyes in a compensatory fashion. In order to assess the degree to which this transformation is evident in vestibular nucleus neuron s of alert cats, we recorded the extracellular discharge properties of 138 second-order vestibular neurons in the superior and medial vestibular nucle us, including 64 neurons identified as second-order vestibulo-ocular neuron s by antidromic responses to oculomotor nucleus stimulation and short-laten cy orthodromic responses to labyrinth stimulation (1.3 ms or less). Neurona l response gains and phases were recorded during 0.5-Hz sinusoidal oscillat ions about many different horizontal axes and during vertical axis rotation s to define neuronal response directionality more precisely than in past st udies. Neurons with spatial responses similar to anterior semicircular cana l afferents were found to have more diverse maximal activation direction ve ctors than neurons with responses resembling those of posterior or horizont al canal afferents. The mean angle from neuron response vector to the axis of the nearest canal or canal pair was 19 degrees for anterior canal second -order neurons (n=28) and 20 degrees for anterior canal second-order vestib ulo-ocular neurons (n=18), compared with 11 degrees for posterior canal sec ond-order neurons (n=43) and 11 degrees for posterior canal second-order ve stibulo-ocular neurons (n=25). Only two second-order vestibulo-ocular neuro ns (3%) showed a marked dependence of response phase on rotation direction, which is indicative of convergent inputs that differ in both dynamics and directionality. This suggests that spatiotemporal convergence is uncommon i n the three-neuron vestibulo-ocular reflex are of the cat. Neuron vectors i ncluded many that were closely aligned with canal axes and several that wer e better aligned with oblique or superior rectus extraocular muscle excitat ion axis vectors. Only single examples of second-order vestibulo-ocular neu ron vectors were approximately aligned with the pitch and roll coordinate a xes. We conclude that second-order vestibulo-ocular neurons do not exclusiv ely represent either the semicircular canal sensory coordinate frame or the extraocular muscle excitation motor coordinate frame, and instead are most ly distributed on a continuum between the input and output coordinate frame s, with anterior canal neurons having the widest distribution of directiona lity.