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Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory

The long-lasting nature of fear memories is essential for survival, but the neural circuitry for retrieval of these associations changes with the passage of time. We previously reported a time-dependent shift from prefrontal-amygdalar circuits to prefrontal-thalamic circuits for the retrieval of aud...

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Autores principales: Quiñones-Laracuente, Kelvin, Vega-Medina, Alexis, Quirk, Gregory 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/PMC8126619/
https://www.ncbi.nlm.nih.gov/pubmed/34012387
http://dx.doi.org/10.3389/fnbeh.2021.665116
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author Quiñones-Laracuente, Kelvin
Vega-Medina, Alexis
Quirk, Gregory J.
author_facet Quiñones-Laracuente, Kelvin
Vega-Medina, Alexis
Quirk, Gregory J.
author_sort Quiñones-Laracuente, Kelvin
collection PubMed
description The long-lasting nature of fear memories is essential for survival, but the neural circuitry for retrieval of these associations changes with the passage of time. We previously reported a time-dependent shift from prefrontal-amygdalar circuits to prefrontal-thalamic circuits for the retrieval of auditory fear conditioning. However, little is known about the time-dependent changes in the originating site, the prefrontal cortex. Here we monitored the responses of prelimbic (PL) prefrontal neurons to conditioned tones at early (2 h) vs. late (4 days) timepoints following training. Using c-Fos, we find that PL neurons projecting to the amygdala are activated early after learning, but not later, whereas PL neurons projecting to the paraventricular thalamus (PVT) show the opposite pattern. Using unit recording, we find that PL neurons in layer V (the origin of projections to amygdala) showed cue-induced excitation at earlier but not later timepoints, whereas PL neurons in Layer VI (the origin of projections to PVT) showed cue-induced inhibition at later, but not earlier, timepoints, along with an increase in spontaneous firing rate. Thus, soon after conditioning, there are conditioned excitatory responses in PL layer V which influence the amygdala. With the passage of time, however, retrieval of fear memories shifts to inhibitory responses in PL layer VI which influence the midline thalamus.
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spelling pubmed-81266192021-05-18 Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory Quiñones-Laracuente, Kelvin Vega-Medina, Alexis Quirk, Gregory J. Front Behav Neurosci Neuroscience The long-lasting nature of fear memories is essential for survival, but the neural circuitry for retrieval of these associations changes with the passage of time. We previously reported a time-dependent shift from prefrontal-amygdalar circuits to prefrontal-thalamic circuits for the retrieval of auditory fear conditioning. However, little is known about the time-dependent changes in the originating site, the prefrontal cortex. Here we monitored the responses of prelimbic (PL) prefrontal neurons to conditioned tones at early (2 h) vs. late (4 days) timepoints following training. Using c-Fos, we find that PL neurons projecting to the amygdala are activated early after learning, but not later, whereas PL neurons projecting to the paraventricular thalamus (PVT) show the opposite pattern. Using unit recording, we find that PL neurons in layer V (the origin of projections to amygdala) showed cue-induced excitation at earlier but not later timepoints, whereas PL neurons in Layer VI (the origin of projections to PVT) showed cue-induced inhibition at later, but not earlier, timepoints, along with an increase in spontaneous firing rate. Thus, soon after conditioning, there are conditioned excitatory responses in PL layer V which influence the amygdala. With the passage of time, however, retrieval of fear memories shifts to inhibitory responses in PL layer VI which influence the midline thalamus. Frontiers Media S.A. 2021-05-03 /pmc/articles/PMC8126619/ /pubmed/34012387 http://dx.doi.org/10.3389/fnbeh.2021.665116 Text en Copyright © 2021 Quiñones-Laracuente, Vega-Medina and Quirk. https://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
Quiñones-Laracuente, Kelvin
Vega-Medina, Alexis
Quirk, Gregory J.
Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title_full Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title_fullStr Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title_full_unstemmed Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title_short Time-Dependent Recruitment of Prelimbic Prefrontal Circuits for Retrieval of Fear Memory
title_sort time-dependent recruitment of prelimbic prefrontal circuits for retrieval of fear memory
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8126619/
https://www.ncbi.nlm.nih.gov/pubmed/34012387
http://dx.doi.org/10.3389/fnbeh.2021.665116
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