Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction

Adverse effects of chronic stress include anxiety, depression, and memory deficits. Some of these stress-induced behavioural deficits are mediated by impaired hippocampal function. Much of our current understanding about how stress affects the hippocampus has been derived from post-mortem analyses o...

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Main Authors: Anupratap Tomar, Denis Polygalov, Sumantra Chattarji, Thomas J. McHugh
Format: Article
Language:English
Published: Elsevier 2021-05-01
Series:Neurobiology of Stress
Subjects:
CA1
Online Access:http://www.sciencedirect.com/science/article/pii/S2352289521000357
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spelling doaj-81392bad35614f7db8cd6fe37d628def2021-05-16T04:23:47ZengElsevierNeurobiology of Stress2352-28952021-05-0114100327Stress enhances hippocampal neuronal synchrony and alters ripple-spike interactionAnupratap Tomar0Denis Polygalov1Sumantra Chattarji2Thomas J. McHugh3Laboratory for Circuit & Behavioral Physiology, RIKEN Center for Brain Science, 2-1 Hirosawa, Wako-shi, Saitama, 351-0021, Japan; Corresponding author.Laboratory for Circuit & Behavioral Physiology, RIKEN Center for Brain Science, 2-1 Hirosawa, Wako-shi, Saitama, 351-0021, JapanNational Centre for Biological Sciences, Bellary Road, Bangalore, 560065, India; Centre for Discovery Brain Sciences, Deanery of Biomedical Sciences, University of Edinburgh, Hugh Robson Building, 15 George Square, Edinburgh, EH89XD, UKLaboratory for Circuit & Behavioral Physiology, RIKEN Center for Brain Science, 2-1 Hirosawa, Wako-shi, Saitama, 351-0021, Japan; Corresponding author.Adverse effects of chronic stress include anxiety, depression, and memory deficits. Some of these stress-induced behavioural deficits are mediated by impaired hippocampal function. Much of our current understanding about how stress affects the hippocampus has been derived from post-mortem analyses of brain slices at fixed time points. Consequently, neural signatures of an ongoing stressful experiences in the intact brain of awake animals and their links to later hippocampal dysfunction remain poorly understood. Further, no information is available on the impact of stress on sharp-wave ripples (SPW-Rs), high frequency oscillation transients crucial for memory consolidation. Here, we used in vivo tetrode recordings to analyze the dynamic impact of 10 days of immobilization stress on neural activity in area CA1 of mice. While there was a net decrease in pyramidal cell activity in stressed animals, a greater fraction of CA1 spikes occurred specifically during sharp-wave ripples, resulting in an increase in neuronal synchrony. After repeated stress some of these alterations were visible during rest even in the absence of stress. These findings offer new insights into stress-induced changes in ripple-spike interactions and mechanisms through which chronic stress may interfere with subsequent information processing.http://www.sciencedirect.com/science/article/pii/S2352289521000357StressHippocampusCA1SPW-RsRipplesPyramidal cells
collection DOAJ
language English
format Article
sources DOAJ
author Anupratap Tomar
Denis Polygalov
Sumantra Chattarji
Thomas J. McHugh
spellingShingle Anupratap Tomar
Denis Polygalov
Sumantra Chattarji
Thomas J. McHugh
Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
Neurobiology of Stress
Stress
Hippocampus
CA1
SPW-Rs
Ripples
Pyramidal cells
author_facet Anupratap Tomar
Denis Polygalov
Sumantra Chattarji
Thomas J. McHugh
author_sort Anupratap Tomar
title Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
title_short Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
title_full Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
title_fullStr Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
title_full_unstemmed Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
title_sort stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
publisher Elsevier
series Neurobiology of Stress
issn 2352-2895
publishDate 2021-05-01
description Adverse effects of chronic stress include anxiety, depression, and memory deficits. Some of these stress-induced behavioural deficits are mediated by impaired hippocampal function. Much of our current understanding about how stress affects the hippocampus has been derived from post-mortem analyses of brain slices at fixed time points. Consequently, neural signatures of an ongoing stressful experiences in the intact brain of awake animals and their links to later hippocampal dysfunction remain poorly understood. Further, no information is available on the impact of stress on sharp-wave ripples (SPW-Rs), high frequency oscillation transients crucial for memory consolidation. Here, we used in vivo tetrode recordings to analyze the dynamic impact of 10 days of immobilization stress on neural activity in area CA1 of mice. While there was a net decrease in pyramidal cell activity in stressed animals, a greater fraction of CA1 spikes occurred specifically during sharp-wave ripples, resulting in an increase in neuronal synchrony. After repeated stress some of these alterations were visible during rest even in the absence of stress. These findings offer new insights into stress-induced changes in ripple-spike interactions and mechanisms through which chronic stress may interfere with subsequent information processing.
topic Stress
Hippocampus
CA1
SPW-Rs
Ripples
Pyramidal cells
url http://www.sciencedirect.com/science/article/pii/S2352289521000357
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