Synaptic Plasticity Can Produce and Enhance Direction Selectivity

Noah J. Cowan,Sean Carver,Eatai Roth,Eric S. Fortune

doi:10.1371/journal.pcbi.0040032

Abstract

The discrimination of the direction of movement of sensory images is critical to the control of many animal behaviors. We propose a parsimonious model of motion processing that generates direction selective responses using short-term synaptic depression and can reproduce salient features of direction selectivity found in a population of neurons in the midbrain of the weakly electric fish Eigenmannia virescens. The model achieves direction selectivity with an elementary Reichardt motion detector: information from spatially separated receptive fields converges onto a neuron via dynamically different pathways. In the model, these differences arise from convergence of information through distinct synapses that either exhibit or do not exhibit short-term synaptic depression—short-term depression produces phase-advances relative to nondepressing synapses. Short-term depression is modeled using two state-variables, a fast process with a time constant on the order of tens to hundreds of milliseconds, and a slow process with a time constant on the order of seconds to tens of seconds. These processes correspond to naturally occurring time constants observed at synapses that exhibit short-term depression. Inclusion of the fast process is sufficient for the generation of temporal disparities that are necessary for direction selectivity in the elementary Reichardt circuit. The addition of the slow process can enhance direction selectivity over time for stimuli that are sustained for periods of seconds or more. Transient (i.e., short-duration) stimuli do not evoke the slow process and therefore do not elicit enhanced direction selectivity. The addition of a sustained global, synchronous oscillation in the gamma frequency range can, however, drive the slow process and enhance direction selectivity to transient stimuli. This enhancement effect does not, however, occur for all combinations of model parameters. The ratio of depressing and nondepressing synapses determines the effects of the addition of the global synchronous oscillation on direction selectivity. These ingredients, short-term depression, spatial convergence, and gamma-band oscillations, are ubiquitous in sensory systems and may be used in Reichardt-style circuits for the generation and enhancement of a variety of biologically relevant spatiotemporal computations.

Highlights

Control of animal behavior often requires the discrimination of the direction of movement of sensory images
We propose a parsimonious model of motion processing using short-term depression to produce directionally selective responses
Information from two spatially separated receptive fields is combined after being asymmetrically processed by synapses that either exhibit short-term synaptic depression or do not

Summary

Introduction

Control of animal behavior often requires the discrimination of the direction of movement of sensory images. A neural correlate of these functions was described over 40 years ago: Hubel and Wiesel characterized central neurons in the mammalian visual system that exhibited preferential responses to particular directions of movement of sensory images [12,13,14] Following this discovery, directionselective response properties have been found in a diversity of animal species and across different sensory modalities, from the visual cortex of cats [12] and somatosensory cortex of monkeys [15] to the electrosensory midbrain of weakly electric fish [16,17]. Of particular interest are the direction selective responses of midbrain neurons observed in a species of weakly electric fish, Eigenmannia virescens These neurons exhibit an unexpected enhancement of direction selectivity by the addition of concomitant naturally occurring sensory oscillations in the gamma frequency range [17]. We propose a parsimonious model to describe and explore the essential features of this mechanism

Results

Discussion

Conclusion