Synaptic plasticity can produce and enhance direction selectivity

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

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
JournalPLoS Computational Biology
Volume4
Issue number2
DOIs
StatePublished - Feb 2008

Fingerprint

Neuronal Plasticity
synapse
Selectivity
Plasticity
plasticity
oscillation
Synapse
Neurons
Synapses
neurons
Time Constant
sensory system
Depression
Networks (circuits)
animal behavior
Oscillation
Fish
detectors
Animals
ingredients

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience
  • Ecology
  • Molecular Biology
  • Genetics
  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Computational Theory and Mathematics

Cite this

Synaptic plasticity can produce and enhance direction selectivity. / Carver, Sean; Roth, Eatai; Cowan, Noah J.; Fortune, Eric S.

In: PLoS Computational Biology, Vol. 4, No. 2, 02.2008.

Research output: Contribution to journalArticle

Carver, Sean ; Roth, Eatai ; Cowan, Noah J. ; Fortune, Eric S. / Synaptic plasticity can produce and enhance direction selectivity. In: PLoS Computational Biology. 2008 ; Vol. 4, No. 2.
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