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Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences

The basolateral nucleus of the amygdala (BL) is thought to support numerous emotional behaviors through specific microcircuits. These are often thought to be comprised of feedforward networks of principal cells (PNs) and interneurons. Neither well-understood nor often considered are recurrent and fe...

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Autores principales: Feng, Feng, Headley, Drew B., Amir, Alon, Kanta, Vasiliki, Chen, Ziao, Paré, Denis, Nair, Satish S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6361623/
https://www.ncbi.nlm.nih.gov/pubmed/30805556
http://dx.doi.org/10.1523/ENEURO.0388-18.2018
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author Feng, Feng
Headley, Drew B.
Amir, Alon
Kanta, Vasiliki
Chen, Ziao
Paré, Denis
Nair, Satish S.
author_facet Feng, Feng
Headley, Drew B.
Amir, Alon
Kanta, Vasiliki
Chen, Ziao
Paré, Denis
Nair, Satish S.
author_sort Feng, Feng
collection PubMed
description The basolateral nucleus of the amygdala (BL) is thought to support numerous emotional behaviors through specific microcircuits. These are often thought to be comprised of feedforward networks of principal cells (PNs) and interneurons. Neither well-understood nor often considered are recurrent and feedback connections, which likely engender oscillatory dynamics within BL. Indeed, oscillations in the gamma frequency range (40 − 100 Hz) are known to occur in the BL, and yet their origin and effect on local circuits remains unknown. To address this, we constructed a biophysically and anatomically detailed model of the rat BL and its local field potential (LFP) based on the physiological and anatomical literature, along with in vivo and in vitro data we collected on the activities of neurons within the rat BL. Remarkably, the model produced intermittent gamma oscillations (∼50 − 70 Hz) whose properties matched those recorded in vivo, including their entrainment of spiking. BL gamma-band oscillations were generated by the intrinsic circuitry, depending upon reciprocal interactions between PNs and fast-spiking interneurons (FSIs), while connections within these cell types affected the rhythm’s frequency. The model allowed us to conduct experimentally impossible tests to characterize the synaptic and spatial properties of gamma. The entrainment of individual neurons to gamma depended on the number of afferent connections they received, and gamma bursts were spatially restricted in the BL. Importantly, the gamma rhythm synchronized PNs and mediated competition between ensembles. Together, these results indicate that the recurrent connectivity of BL expands its computational and communication repertoire.
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spelling pubmed-63616232019-02-25 Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences Feng, Feng Headley, Drew B. Amir, Alon Kanta, Vasiliki Chen, Ziao Paré, Denis Nair, Satish S. eNeuro New Research The basolateral nucleus of the amygdala (BL) is thought to support numerous emotional behaviors through specific microcircuits. These are often thought to be comprised of feedforward networks of principal cells (PNs) and interneurons. Neither well-understood nor often considered are recurrent and feedback connections, which likely engender oscillatory dynamics within BL. Indeed, oscillations in the gamma frequency range (40 − 100 Hz) are known to occur in the BL, and yet their origin and effect on local circuits remains unknown. To address this, we constructed a biophysically and anatomically detailed model of the rat BL and its local field potential (LFP) based on the physiological and anatomical literature, along with in vivo and in vitro data we collected on the activities of neurons within the rat BL. Remarkably, the model produced intermittent gamma oscillations (∼50 − 70 Hz) whose properties matched those recorded in vivo, including their entrainment of spiking. BL gamma-band oscillations were generated by the intrinsic circuitry, depending upon reciprocal interactions between PNs and fast-spiking interneurons (FSIs), while connections within these cell types affected the rhythm’s frequency. The model allowed us to conduct experimentally impossible tests to characterize the synaptic and spatial properties of gamma. The entrainment of individual neurons to gamma depended on the number of afferent connections they received, and gamma bursts were spatially restricted in the BL. Importantly, the gamma rhythm synchronized PNs and mediated competition between ensembles. Together, these results indicate that the recurrent connectivity of BL expands its computational and communication repertoire. Society for Neuroscience 2019-02-05 /pmc/articles/PMC6361623/ /pubmed/30805556 http://dx.doi.org/10.1523/ENEURO.0388-18.2018 Text en Copyright © 2019 Feng et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle New Research
Feng, Feng
Headley, Drew B.
Amir, Alon
Kanta, Vasiliki
Chen, Ziao
Paré, Denis
Nair, Satish S.
Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title_full Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title_fullStr Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title_full_unstemmed Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title_short Gamma Oscillations in the Basolateral Amygdala: Biophysical Mechanisms and Computational Consequences
title_sort gamma oscillations in the basolateral amygdala: biophysical mechanisms and computational consequences
topic New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6361623/
https://www.ncbi.nlm.nih.gov/pubmed/30805556
http://dx.doi.org/10.1523/ENEURO.0388-18.2018
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