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High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear

The hippocampus can be divided into distinct segments that make unique contributions to learning and memory. The dorsal segment supports cognitive processes like spatial learning and navigation while the ventral hippocampus regulates emotional behaviors related to fear, anxiety and reward. In the cu...

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Autores principales: Graham, Jalina, D’Ambra, Alexa F., Jung, Se Jung, Teratani-Ota, Yusuke, Vishwakarma, Nina, Venkatesh, Rasika, Parigi, Abhijna, Antzoulatos, Evan G., Fioravante, Diasynou, Wiltgen, Brian J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985556/
https://www.ncbi.nlm.nih.gov/pubmed/33767614
http://dx.doi.org/10.3389/fnbeh.2021.595049
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author Graham, Jalina
D’Ambra, Alexa F.
Jung, Se Jung
Teratani-Ota, Yusuke
Vishwakarma, Nina
Venkatesh, Rasika
Parigi, Abhijna
Antzoulatos, Evan G.
Fioravante, Diasynou
Wiltgen, Brian J.
author_facet Graham, Jalina
D’Ambra, Alexa F.
Jung, Se Jung
Teratani-Ota, Yusuke
Vishwakarma, Nina
Venkatesh, Rasika
Parigi, Abhijna
Antzoulatos, Evan G.
Fioravante, Diasynou
Wiltgen, Brian J.
author_sort Graham, Jalina
collection PubMed
description The hippocampus can be divided into distinct segments that make unique contributions to learning and memory. The dorsal segment supports cognitive processes like spatial learning and navigation while the ventral hippocampus regulates emotional behaviors related to fear, anxiety and reward. In the current study, we determined how pyramidal cells in ventral CA1 respond to spatial cues and aversive stimulation during a context fear conditioning task. We also examined the effects of high and low frequency stimulation of these neurons on defensive behavior. Similar to previous work in the dorsal hippocampus, we found that cells in ventral CA1 expressed high-levels of c-Fos in response to a novel spatial environment. Surprisingly, however, the number of activated neurons did not increase when the environment was paired with footshock. This was true even in the subpopulation of ventral CA1 pyramidal cells that send direct projections to the amygdala. When these cells were stimulated at high-frequencies (20 Hz) we observed feedforward inhibition of basal amygdala neurons and impaired expression of context fear. In contrast, low-frequency stimulation (4 Hz) did not inhibit principal cells in the basal amygdala and produced an increase in fear generalization. Similar results have been reported in dorsal CA1. Therefore, despite clear differences between the dorsal and ventral hippocampus, CA1 neurons in each segment appear to make similar contributions to context fear conditioning.
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spelling pubmed-79855562021-03-24 High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear Graham, Jalina D’Ambra, Alexa F. Jung, Se Jung Teratani-Ota, Yusuke Vishwakarma, Nina Venkatesh, Rasika Parigi, Abhijna Antzoulatos, Evan G. Fioravante, Diasynou Wiltgen, Brian J. Front Behav Neurosci Neuroscience The hippocampus can be divided into distinct segments that make unique contributions to learning and memory. The dorsal segment supports cognitive processes like spatial learning and navigation while the ventral hippocampus regulates emotional behaviors related to fear, anxiety and reward. In the current study, we determined how pyramidal cells in ventral CA1 respond to spatial cues and aversive stimulation during a context fear conditioning task. We also examined the effects of high and low frequency stimulation of these neurons on defensive behavior. Similar to previous work in the dorsal hippocampus, we found that cells in ventral CA1 expressed high-levels of c-Fos in response to a novel spatial environment. Surprisingly, however, the number of activated neurons did not increase when the environment was paired with footshock. This was true even in the subpopulation of ventral CA1 pyramidal cells that send direct projections to the amygdala. When these cells were stimulated at high-frequencies (20 Hz) we observed feedforward inhibition of basal amygdala neurons and impaired expression of context fear. In contrast, low-frequency stimulation (4 Hz) did not inhibit principal cells in the basal amygdala and produced an increase in fear generalization. Similar results have been reported in dorsal CA1. Therefore, despite clear differences between the dorsal and ventral hippocampus, CA1 neurons in each segment appear to make similar contributions to context fear conditioning. Frontiers Media S.A. 2021-03-09 /pmc/articles/PMC7985556/ /pubmed/33767614 http://dx.doi.org/10.3389/fnbeh.2021.595049 Text en Copyright © 2021 Graham, D’Ambra, Jung, Teratani-Ota, Vishwakarma, Venkatesh, Parigi, Antzoulatos, Fioravante and Wiltgen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Graham, Jalina
D’Ambra, Alexa F.
Jung, Se Jung
Teratani-Ota, Yusuke
Vishwakarma, Nina
Venkatesh, Rasika
Parigi, Abhijna
Antzoulatos, Evan G.
Fioravante, Diasynou
Wiltgen, Brian J.
High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title_full High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title_fullStr High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title_full_unstemmed High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title_short High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
title_sort high-frequency stimulation of ventral ca1 neurons reduces amygdala activity and inhibits fear
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7985556/
https://www.ncbi.nlm.nih.gov/pubmed/33767614
http://dx.doi.org/10.3389/fnbeh.2021.595049
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