Influence of eye position on activity in monkey superior colliculus.

1. Most recording studies on the role of the monkey superior colliculus (SC) in eye movement generation have so far indicated that the code of the recruited population of cells is a fixed vector command representing the desired saccadic eye displacement vector, irrespective of the position of the eyes in the orbit. Experimental evidence from microstimulation, lesions, and neuroanatomy, however, suggests that the SC may have access to an eye position signal. 2. In this paper we have tested the hypothesis that SC activity is influenced by eye position, by recording from presaccadic burst neurons while monkeys made rapid eye movements in the light covering a large part of the oculomotor range. 3. In four alert rhesus monkeys, we obtained sufficient data from 57 SC single units. The activity of a substantial part of these cells (30/57) appeared to be significantly influenced by eye position. Although the tuning properties of these cells for saccade amplitude and direction remained invariant for changes in eye position, the peak firing rate of these units was systematically influenced by the position of the eyes in the head. 4. We have characterized this eye position dependence of a neuron's activity by a qualitative, model-independent, as well as by a quantitative model description (gain field), which takes into account both the tuning properties of the cell for eye displacement vectors and the dependence of eye position. 5. Although a majority of gain fields had their eye position sensitivity vector roughly aligned with the optimal saccade vector direction (colinear gain field, 17/30), a substantial part of the gain fields had their eye position sensitivity vectors in quite different directions, approximately homogeneously distributed with respect to the cell's ON direction. 6. We conclude that the SC has access to a signal related to the position of the eyes in the orbit. Several hypotheses on the possible functional role of this signal, in relation to the neural code of the motor map, are discussed.