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Descending pathways generate perception of and neural responses to weak sensory input

Metzen, MG; Huang, CG; Chacron, MJ; (2018) Descending pathways generate perception of and neural responses to weak sensory input. PLoS Biology , 16 (6) , Article e2005239. 10.1371/journal.pbio.2005239. Green open access

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Abstract

Natural sensory stimuli frequently consist of a fast time-varying waveform whose amplitude or contrast varies more slowly. While changes in contrast carry behaviorally relevant information necessary for sensory perception, their processing by the brain remains poorly understood to this day. Here, we investigated the mechanisms that enable neural responses to and perception of low-contrast stimuli in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. We found that fish reliably detected such stimuli via robust behavioral responses. Recordings from peripheral electrosensory neurons revealed stimulus-induced changes in firing activity (i.e., phase locking) but not in their overall firing rate. However, central electrosensory neurons receiving input from the periphery responded robustly via both phase locking and increases in firing rate. Pharmacological inactivation of feedback input onto central electrosensory neurons eliminated increases in firing rate but did not affect phase locking for central electrosensory neurons in response to low-contrast stimuli. As feedback inactivation eliminated behavioral responses to these stimuli as well, our results show that it is changes in central electrosensory neuron firing rate that are relevant for behavior, rather than phase locking. Finally, recordings from neurons projecting directly via feedback to central electrosensory neurons revealed that they provide the necessary input to cause increases in firing rate. Our results thus provide the first experimental evidence that feedback generates both neural and behavioral responses to low-contrast stimuli that are commonly found in the natural environment.

Type: Article
Title: Descending pathways generate perception of and neural responses to weak sensory input
Open access status: An open access version is available from UCL Discovery
DOI: 10.1371/journal.pbio.2005239
Publisher version: https://doi.org/10.1371/journal.pbio.2005239
Language: English
Additional information: © 2018 Metzen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (https://doi.org/10.1371/journal.pbio.2005239).
Keywords: Neurons, Animal behavior, Sensory perception, Pyramidal cells, Brain, Action potentials, Phase determination, Signal processing
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > The Ear Institute
URI: https://discovery.ucl.ac.uk/id/eprint/10061223
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