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Tactile frequency discrimination is enhanced by circumventing neocortical adaptation


Musall, Simon; von der Behrens, Wolfger; Mayrhofer, Johannes M; Weber, Bruno; Helmchen, Fritjof; Haiss, Florent (2014). Tactile frequency discrimination is enhanced by circumventing neocortical adaptation. Nature Neuroscience, 17(11):1567-1573.

Abstract

Neocortical responses typically adapt to repeated sensory stimulation, improving sensitivity to stimulus changes, but possibly also imposing limitations on perception. For example, it is unclear whether information about stimulus frequency is perturbed by adaptation or encoded by precise response timing. We addressed this question in rat barrel cortex by comparing performance in behavioral tasks with either whisker stimulation, which causes frequency-dependent adaptation, or optical activation of cortically expressed channelrhodopsin-2, which elicits non-adapting neural responses. Circumventing adaption by optical activation substantially improved cross-hemispheric discrimination of stimulus frequency. This improvement persisted when temporal precision of optically evoked spikes was reduced. We were able to replicate whisker-driven behavior only by applying adaptation rules mimicking sensory-evoked responses to optical stimuli. Conversely, in a change-detection task, animals performed better with whisker than optical stimulation. Our results directly demonstrate that sensory adaptation critically governs the perception of stimulus patterns, decreasing fidelity under steady-state conditions in favor of change detection.

Abstract

Neocortical responses typically adapt to repeated sensory stimulation, improving sensitivity to stimulus changes, but possibly also imposing limitations on perception. For example, it is unclear whether information about stimulus frequency is perturbed by adaptation or encoded by precise response timing. We addressed this question in rat barrel cortex by comparing performance in behavioral tasks with either whisker stimulation, which causes frequency-dependent adaptation, or optical activation of cortically expressed channelrhodopsin-2, which elicits non-adapting neural responses. Circumventing adaption by optical activation substantially improved cross-hemispheric discrimination of stimulus frequency. This improvement persisted when temporal precision of optically evoked spikes was reduced. We were able to replicate whisker-driven behavior only by applying adaptation rules mimicking sensory-evoked responses to optical stimuli. Conversely, in a change-detection task, animals performed better with whisker than optical stimulation. Our results directly demonstrate that sensory adaptation critically governs the perception of stimulus patterns, decreasing fidelity under steady-state conditions in favor of change detection.

Citations

15 citations in Web of Science®
11 citations in Scopus®
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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Institute of Pharmacology and Toxicology
07 Faculty of Science > Institute of Neuroinformatics
04 Faculty of Medicine > Brain Research Institute
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Language:English
Date:November 2014
Deposited On:20 Feb 2015 11:05
Last Modified:05 Apr 2016 18:56
Publisher:Nature Publishing Group
ISSN:1097-6256
Publisher DOI:https://doi.org/10.1038/nn.3821
PubMed ID:25242306

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