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Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection

Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell’s dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending...

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Autores principales: Dewell, Richard Burkett, Zhu, Ying, Eisenbrandt, Margaret, Morse, Richard, Gabbiani, Fabrizio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9674337/
https://www.ncbi.nlm.nih.gov/pubmed/36314775
http://dx.doi.org/10.7554/eLife.79772
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author Dewell, Richard Burkett
Zhu, Ying
Eisenbrandt, Margaret
Morse, Richard
Gabbiani, Fabrizio
author_facet Dewell, Richard Burkett
Zhu, Ying
Eisenbrandt, Margaret
Morse, Richard
Gabbiani, Fabrizio
author_sort Dewell, Richard Burkett
collection PubMed
description Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell’s dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending collision. In response to black approaching objects, the neuron receives OFF excitatory inputs that form a retinotopic map of the visual field onto compartmentalized, distal dendrites. Subsequent processing of these OFF inputs by active membrane conductances allows the neuron to discriminate the spatial coherence of such stimuli. In contrast, we show that ON excitatory synaptic inputs activated by white approaching objects map in a random manner onto a more proximal dendritic field of the same neuron. The lack of retinotopic synaptic arrangement results in the neuron’s inability to discriminate the coherence of white approaching stimuli. Yet, the neuron retains the ability to discriminate stimulus coherence for checkered stimuli of mixed ON/OFF polarity. The coarser mapping and processing of ON stimuli thus has a minimal impact, while reducing the total energetic cost of the circuit. Further, we show that these differences in ON/OFF neuronal processing are behaviorally relevant, being tightly correlated with the animal’s escape behavior to light and dark stimuli of variable coherence. Our results show that the synaptic mapping of excitatory inputs affects the fine stimulus discrimination ability of single neurons and document the resulting functional impact on behavior.
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spelling pubmed-96743372022-11-19 Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection Dewell, Richard Burkett Zhu, Ying Eisenbrandt, Margaret Morse, Richard Gabbiani, Fabrizio eLife Neuroscience Neurons receive information through their synaptic inputs, but the functional significance of how those inputs are mapped on to a cell’s dendrites remains unclear. We studied this question in a grasshopper visual neuron that tracks approaching objects and triggers escape behavior before an impending collision. In response to black approaching objects, the neuron receives OFF excitatory inputs that form a retinotopic map of the visual field onto compartmentalized, distal dendrites. Subsequent processing of these OFF inputs by active membrane conductances allows the neuron to discriminate the spatial coherence of such stimuli. In contrast, we show that ON excitatory synaptic inputs activated by white approaching objects map in a random manner onto a more proximal dendritic field of the same neuron. The lack of retinotopic synaptic arrangement results in the neuron’s inability to discriminate the coherence of white approaching stimuli. Yet, the neuron retains the ability to discriminate stimulus coherence for checkered stimuli of mixed ON/OFF polarity. The coarser mapping and processing of ON stimuli thus has a minimal impact, while reducing the total energetic cost of the circuit. Further, we show that these differences in ON/OFF neuronal processing are behaviorally relevant, being tightly correlated with the animal’s escape behavior to light and dark stimuli of variable coherence. Our results show that the synaptic mapping of excitatory inputs affects the fine stimulus discrimination ability of single neurons and document the resulting functional impact on behavior. eLife Sciences Publications, Ltd 2022-10-31 /pmc/articles/PMC9674337/ /pubmed/36314775 http://dx.doi.org/10.7554/eLife.79772 Text en © 2022, Dewell, Zhu et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Dewell, Richard Burkett
Zhu, Ying
Eisenbrandt, Margaret
Morse, Richard
Gabbiani, Fabrizio
Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title_full Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title_fullStr Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title_full_unstemmed Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title_short Contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
title_sort contrast polarity-specific mapping improves efficiency of neuronal computation for collision detection
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9674337/
https://www.ncbi.nlm.nih.gov/pubmed/36314775
http://dx.doi.org/10.7554/eLife.79772
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