Abstract

An animal’s motion through the environment can induce large and frequent fluctuations in light intensity on the retina. These fluctuations pose a major challenge to neural circuits tasked with encoding visual information, as they can cause cells to adapt and lose sensitivity. Here, we report that sensitization, a short-term plasticity mechanism, solves this difficult computational problem by maintaining neuronal sensitivity in the face of these fluctuations. The numerically dominant output pathway in the macaque monkey retina, the midget (parvocellular-projecting) pathway, undergoes sensitization under specific conditions, including simulated eye movements. Sensitization is present in the excitatory synaptic inputs from midget bipolar cells and is mediated by presynaptic disinhibition from a wide-field mechanism extending >0.5 mm along the retinal surface. Direct physiological recordings and a computational model indicate that sensitization in the midget pathway supports accurate sensory encoding and prevents a loss of responsiveness during dynamic visual processing.

Highlights

  • An animal’s motion through the environment can induce large and frequent fluctuations in light intensity on the retina

  • A computational model based on synaptic input recordings further indicated that this increase in sensitivity greatly enhanced the fidelity of encoding natural scenes

  • –0.5 0 0.5 Negative contrast recordings—the adapting stimulus evoked a leftward shift in the contrast-response curve relative to the unadapted control (Fig. 7b). These results indicated that contrast sensitization was present in the excitatory synaptic input from midget bipolar cells to midget ganglion cells

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Summary

Introduction

An animal’s motion through the environment can induce large and frequent fluctuations in light intensity on the retina. Given that neural sensitization was only recently discovered, relatively little is known about its roles in neural information processing To address this issue, we recorded from five types of output neurons in the macaque monkey retina—broad thorny (koniocellular-projecting), On and Off parasol (magnocellular-projecting), and On and Off midget (parvocellular-projecting) ganglion cells. We recorded from five types of output neurons in the macaque monkey retina—broad thorny (koniocellular-projecting), On and Off parasol (magnocellular-projecting), and On and Off midget (parvocellular-projecting) ganglion cells These cells have well described roles in visual processing and no known functional counterparts. The lack of an adapting counterpart to midget cells indicated that sensitizing circuits performed a distinct role in primate retina relative to that observed in other vertebrate neural systems[10,11,12,16]

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