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The Journal of Neuroscience, November 26, 2003, 23(34):10852-10858

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Behavioral/Systems/Cognitive
Correlated Discharge among Cell Pairs within the Oculomotor Horizontal Velocity-to-Position Integrator

Emre Aksay,¹ Robert Baker,² H. Sebastian Seung,³ and David W. Tank¹

¹Departments of Molecular Biology and Physics, Princeton University, Princeton, New Jersey 08544, ²Department of Physiology and Neuroscience, New York University Medical Center, New York, New York 10016, and ³Howard Hughes Medical Institute, Brain and Cognitive Sciences Department, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

In the oculomotor system, temporal integration of velocity commands into position signals may depend on synaptic feedback among neurons of a bilateral brainstem cell assembly known as the "neural integrator." Both ipsilateral excitatory and contralateral inhibitory projections between eye position-related integrator cells are hypothesized as a substrate for positive feedback supporting integration. Presence of feedback interactions should be evident in cross-correlation functions of neuron pairs. Here, unilateral and bilateral paired recordings were obtained during fixation behavior from neurons in goldfish brainstem area I, a key element of the integrator. During fixations, discharge of most unilateral pairs, composed of cells with eye position sensitivities of the same sign, was positively correlated with lag of 0-10 msec (n = 11 of 14 significant). Typically, a very narrow peak (mean half-width <4 msec) near zero lag was observed. Discharge of bilateral pairs, composed of cells with position sensitivities of the opposite sign, was either negatively correlated with lag of 0-10 msec (n = 5 of 13 significant) or not correlated. Troughs in negative correlations always had minima between 3 and 5 msec lag. These results are consistent with the feedback hypothesis of temporal integration, highlighting excitation unilaterally and inhibition bilaterally. Absence of visual input did not weaken correlations, but other sources of correlated input extrinsic to area I were not ruled out. Triplet recordings revealed that unilateral pairwise correlations were primarily independent. Correlation between unilateral pairs systematically decreased with increasing eye position, demonstrating that synchrony is not necessary for persistent activity at high firing rates.

Key words: eye position; fixation; memory; integrator; synchrony; persistence

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Received July 16, 2003; revised September 19, 2003; accepted September 23, 2003.

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