Abstract

The midbrain superior colliculus (SC) is a crucial sensorimotor interface in the generation of rapid saccadic gaze shifts. For every saccade it recruits a large population of cells in its vectorial motor map. Supra-threshold electrical microstimulation in the SC reveals that the stimulated site produces the saccade vector specified by the motor map. Electrically evoked saccades (E-saccades) have kinematic properties that strongly resemble natural, visual-evoked saccades (V-saccades), with little influence of the stimulation parameters. Moreover, synchronous stimulation at two sites yields eye movements that resemble a weighted vector average of the individual stimulation effects. Single-unit recordings have indicated that the SC population acts as a vectorial pulse generator by specifying the instantaneous gaze-kinematics through dynamic summation of the movement effects of all SC spike trains. But how to reconcile the a-specific stimulation pulses with these intricate saccade properties? We recently developed a spiking neural network model of the SC, in which microstimulation initially activates a relatively small set of (~50) neurons around the electrode tip, which subsequently sets up a large population response (~5,000 neurons) through lateral synaptic interactions. Single-site microstimulation in this network thus produces the saccade properties and firing rate profiles as seen in single-unit recording experiments. We here show that this mechanism also accounts for many results of simultaneous double stimulation at different SC sites. The resulting E-saccade trajectories resemble a weighted average of the single-site effects, in which stimulus current strength of the electrode pulses serve as weighting factors. We discuss under which conditions the network produces effects that deviate from experimental results.

Highlights

  • Superior ColliculusBecause high spatial resolution is limited to the central fovea, the primate visual system needs to explore the environment through rapid and precise saccadic eye movements

  • We show that linear dynamic ensemble-coding with lateral excitatory-inhibitory interactions in the motor map can account for most of the experimental vector-averaging results to double stimulation [9, 20, 35], without the need for additional computational nonlinearities, such as a downstream population center-of-gravity computation [20, 21, 34], or a spike-counting cut-off threshold [13, 39, 40]

  • Synchronous double stimulation in a spiking neural network model of the superior colliculus (SC) with Gaussian excitatory-inhibitory interactions results in saccade responses that display many of the features that have been reported in electrophysiological studies [9, 25, 34]: when the electrodes were located on an iso-direction line (v = constant) the resulting saccade amplitudes were a weighted average of the individual stimulus effects, with the current strengths acting as weighting parameters (Figures 5– 8)

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Summary

INTRODUCTION

Because high spatial resolution is limited to the central fovea, the primate visual system needs to explore the environment through rapid and precise saccadic eye movements. We implemented a simple spiking neural network model for the SC that can generate realistic saccades to visual targets [23] This minimalistic (one-dimensional) model with lateral excitatory-inhibitory interactions among the SC cells accounts for most of the experimentally observed firing properties of saccade-related neurons in the motor map [8, 13], and yields saccades with normal main-sequence properties. We show that linear dynamic ensemble-coding with lateral excitatory-inhibitory interactions in the motor map can account for most of the experimental vector-averaging results to double stimulation [9, 20, 35], without the need for additional computational nonlinearities, such as a downstream population center-of-gravity computation [20, 21, 34], or a spike-counting cut-off threshold [13, 39, 40]. We discuss to what extent the model’s responses deviate from experimental findings, and suggest some further refinements to the model

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