Local population synchrony and the encoding of eye position in the primate neural integrator

Abstract

Encoding horizontal eye position in the oculomotor system occurs through temporal integration of eye velocity inputs to produce tonic outputs. The nucleus prepositus is commonly believed to be the “neural integrator” that accomplishes this function through the activity of its ensemble of predominantly burst-tonic neurons. Single-unit characterizations and labeling studies of these neurons have suggested that their collective output is achieved through local feedback loops produced by direct connections between them. If this is the case, then the ensemble of burst-tonic neurons should exhibit correlated activity. To obtain electrophysiological evidence of local interactions between neurons, we simultaneously recorded pairs (n = 29) of burst-tonic neurons in the nucleus prepositus of rhesus macaque monkeys using eight-channel linear microelectrode arrays. We computed the magnitude of synchrony between their spike trains as a function of eye position during ocular fixations and as a function of distance between neurons. Importantly, we found that neurons exhibit unexpected levels of positive synchrony, which is maximal during contralateral fixations and weakest when neurons are located far apart from one another (>300 μm). Together, our results support a role for shared inputs to ipsilateral pairs of burst-tonic neurons in the encoding of eye position in the primate nucleus prepositus.