Anterior canal neurons in cat vestibular nuclei have large phase leads during low frequency vertical axis pitch

Vestibulo-ocular and second-order neurons in medial and superior vestibular nuclei of alert cats were identified by antidromic and orthodromic electrical stimulation, and their responses to whole body rotations were recorded in the dark. Neurons that had spatial sensitivity most closely aligned with the anterior canal (anterior canal neurons) were compared with neurons that had spatial sensitivity most closely aligned with the posterior canal (posterior canal neurons). Responses were recorded during low frequency earth-horizontal axis pitch rotations in the normal upright posture, and during earth-vertical axis pitch with the head and body lying on the left side. During upright pitch, response phases of anterior canal neurons slightly lagged those of posterior canal neurons or primary vestibular afferents, as previously reported. During on-side pitch, anterior canal neurons showed far greater phase leads with respect to head velocity than posterior canal neurons, primary vestibular afferents, or previously reported vestibulo-ocular reflex eye movements. These results provide challenges for vestibulo-ocular reflex models to incorporate central mechanisms for phase leads among the inputs to anterior canal neurons and to explain how the anterior canal neuron signals reported here combine with other signals to produce observed vestibulo-ocular reflex behavior.