Linear integration of convergent visual inputs in an oculomotor reflex pathway.

The functional connectivity between identified visual interneurons [sustaining fibers (SF)] and oculomotor neurons was assessed by simultaneous recording and cross-correlation analysis. A small group of SFs exhibit excitatory functional connections to an identified tonic oculomotor neuron. The excitatory interactions are found exclusively between SFs and oculomotor neurons with similar and/or overlapping excitatory receptive fields. A second group of SFs exhibit inhibitory connections to motor neurons. The excitatory receptive fields of these SFs correspond to the inhibitory receptive fields of the motor neurons. The collective action of the SFs is sufficient to produce all of the steady-state visual behavior of the motor neurons including the increment in firing rate elicited by illumination, unique features of the motor neuron receptive field, and differential sensitivity to blue light and polarized light. Pairs of SFs that converge on the same motor neuron sum their effects linearly. Thus the joint interaction of two SFs on a motor neuron is equal to the sum of the two postsynaptic effects taken separately. Coactivation of excitatory and inhibitory SF inputs to a motor neuron results in a partial cancellation of their postsynaptic effects on the motor neuron's firing rate. The antagonistic interactions protect the system from perturbations by stray light, visual adaptation, and variations in the central excited state. The ensemble information code, at the SF level of the optomotor pathway, is a set of differentially weighted mean firing rates. The weightings reflect differences in the strengths of the several SF-to- motor neuron interactions. One consequence of these differences is a selective weighting of the effects of illumination (in different regions of visual space) on the compensatory eye reflex.