Characterization of Purkinje cells in the goldfish cerebellum during eye movement and adaptive modification of the vestibulo-ocular reflex.

The discharge characteristics of Purkinje cells were analyzed in the goldfish cerebellum during eye movement and adaptation of the vestibulo-ocular reflex (VOR). Purkinje cells, identified by the simultaneous recording of complex and simple spikes, were recorded in the cerebellar area where electrical microstimulation elicited ipsiversive horizontal eye movements. Simple spikes of Purkinje cells displayed signals related to head and/or eye velocity as determined independently during either VOR suppression or optokinetic stimulation, respectively. Head velocity-only Purkinje cells (12%) increased their firing rate in relationship to ipsilateral head movements. Two types of eye velocity-only Purkinje cells (28%) were found that responded either in phase with ipsi- (16%) or contralateral (12%) eye movement, respectively. Purkinje cells combining both eye and head velocity (60%) were classified into two groups according to their preferred direction for eye movement. Eye velocity signals either added to (18%) or subtracted from (42%) head velocity during all visuo-vestibular interactions. Short term adaptive changes of the VOR were induced by oscillating goldfish in a moving visual surround that modified the ratio of eye to head velocity (gain) from a level of 1.0 (16 degrees/s) towards gains ranging from 2.5 (40 degrees/s) to -1.0 (-16 degrees/s). Simple spike modulation of individual Purkinje cells was shown to correlate well with VOR performance throughout adaptation irrespective of training direction. Purkinje cell behavior always equaled the algebraic summation of eye and head velocity signal sensitivity. Causality of signal generation was addressed by measuring Purkinje cell responses to both eye and head velocity separately throughout the time course of VOR adaptation. The sensitivity of each type of Purkinje cell was found to be independent of the VOR gain state. We therefore conclude that the changes responsible for short term VOR plasticity do not occur in the cerebellum. These observations suggest that Purkinje cells integrate corollary head and eye velocity signals to continuously adjust the set point of brainstem VOR interneurons that embrace the substantive site for adaptive plasticity.