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Linear Summation Underlies Direction Selectivity in Drosophila.

ABSTRACT: While linear mechanisms lay the foundations of feature selectivity in many brain areas, direction selectivity in the elementary motion detector (EMD) of the fly has become a paradigm of nonlinear neuronal computation. We have bridged this divide by demonstrating that linear spatial summation can generate direction selectivity in the fruit fly Drosophila. Using linear systems analysis and two-photon imaging of a genetically encoded voltage indicator, we measure the emergence of direction-selective (DS) voltage signals in the Drosophila OFF pathway. Our study is a direct, quantitative investigation of the algorithm underlying directional signals, with the striking finding that linear spatial summation is sufficient for the emergence of direction selectivity. A linear stage of the fly EMD strongly resembles similar computations in vertebrate visual cortex, demands a reappraisal of the role of upstream nonlinearities, and implicates the voltage-to-calcium transformation in the refinement of feature selectivity in this system. VIDEO ABSTRACT.

SUBMITTER: Wienecke CFR

PROVIDER: S-EPMC6107374 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Linear Summation Underlies Direction Selectivity in Drosophila.

Wienecke Carl F R CFR Leong Jonathan C S JCS Clandinin Thomas R TR

Neuron 20180726 4

While linear mechanisms lay the foundations of feature selectivity in many brain areas, direction selectivity in the elementary motion detector (EMD) of the fly has become a paradigm of nonlinear neuronal computation. We have bridged this divide by demonstrating that linear spatial summation can generate direction selectivity in the fruit fly Drosophila. Using linear systems analysis and two-photon imaging of a genetically encoded voltage indicator, we measure the emergence of direction-selectiv ...[more]

PMID: 30057202

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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

Linear Summation Underlies Direction Selectivity in Drosophila.

Publications

Linear Summation Underlies Direction Selectivity in Drosophila.

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