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Synaptic plasticity and connectivity requirements to produce stimulus-pair specific responses in recurrent networks of spiking neurons.

ABSTRACT: Animals must respond selectively to specific combinations of salient environmental stimuli in order to survive in complex environments. A task with these features, biconditional discrimination, requires responses to select pairs of stimuli that are opposite to responses to those stimuli in another combination. We investigate the characteristics of synaptic plasticity and network connectivity needed to produce stimulus-pair neural responses within randomly connected model networks of spiking neurons trained in biconditional discrimination. Using reward-based plasticity for synapses from the random associative network onto a winner-takes-all decision-making network representing perceptual decision-making, we find that reliably correct decision making requires upstream neurons with strong stimulus-pair selectivity. By chance, selective neurons were present in initial networks; appropriate plasticity mechanisms improved task performance by enhancing the initial diversity of responses. We find long-term potentiation of inhibition to be the most beneficial plasticity rule by suppressing weak responses to produce reliably correct decisions across an extensive range of networks.

SUBMITTER: Bourjaily MA

PROVIDER: S-EPMC3044762 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Synaptic plasticity and connectivity requirements to produce stimulus-pair specific responses in recurrent networks of spiking neurons.

Bourjaily Mark A MA Miller Paul P

PLoS computational biology 20110224 2

Animals must respond selectively to specific combinations of salient environmental stimuli in order to survive in complex environments. A task with these features, biconditional discrimination, requires responses to select pairs of stimuli that are opposite to responses to those stimuli in another combination. We investigate the characteristics of synaptic plasticity and network connectivity needed to produce stimulus-pair neural responses within randomly connected model networks of spiking neur ...[more]

PMID: 21390275

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Project description: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.

Dataset Information

Synaptic plasticity and connectivity requirements to produce stimulus-pair specific responses in recurrent networks of spiking neurons.

Publications

Synaptic plasticity and connectivity requirements to produce stimulus-pair specific responses in recurrent networks of spiking neurons.

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