Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice

Ascending serotonergic/glutamatergic projection from the median raphe region (MRR) to the hippocampal formation regulates both encoding and consolidation of memory and the oscillations associated with them. The firing of various types of MRR neurons exhibits rhythmic modulation coupled to hippocampa...

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Main Authors: Marta Jelitai, Albert M. Barth, Ferenc Komlósi, Tamás F. Freund, Viktor Varga
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncir.2021.784034/full
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author Marta Jelitai
Albert M. Barth
Ferenc Komlósi
Tamás F. Freund
Viktor Varga
author_facet Marta Jelitai
Albert M. Barth
Ferenc Komlósi
Tamás F. Freund
Viktor Varga
author_sort Marta Jelitai
collection DOAJ
description Ascending serotonergic/glutamatergic projection from the median raphe region (MRR) to the hippocampal formation regulates both encoding and consolidation of memory and the oscillations associated with them. The firing of various types of MRR neurons exhibits rhythmic modulation coupled to hippocampal oscillatory activity. A possible intermediary between rhythm-generating forebrain regions and entrained ascending modulation may be the GABAergic circuit in the MRR, known to be targeted by a diverse array of top-down inputs. However, the activity of inhibitory MRR neurons in an awake animal is still largely unexplored. In this study, we utilized whole cell patch-clamp, single cell, and multichannel extracellular recordings of GABAergic and non-GABAergic MRR neurons in awake, head-fixed mice. First, we have demonstrated that glutamatergic and serotonergic neurons receive both transient, phasic, and sustained tonic inhibition. Then, we observed substantial heterogeneity of GABAergic firing patterns but a marked modulation of activity by brain states and fine timescale coupling of spiking to theta and ripple oscillations. We also uncovered a correlation between the preferred theta phase and the direction of activity change during ripples, suggesting the segregation of inhibitory neurons into functional groups. Finally, we could detect complementary alteration of non-GABAergic neurons’ ripple-coupled activity. Our findings support the assumption that the local inhibitory circuit in the MRR may synchronize ascending serotonergic/glutamatergic modulation with hippocampal activity on a subsecond timescale.
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spelling doaj.art-3d1fd5076c3a4ba4996b5af9b80c8a3f2022-12-21T19:23:06ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102021-12-011510.3389/fncir.2021.784034784034Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake MiceMarta Jelitai0Albert M. Barth1Ferenc Komlósi2Tamás F. Freund3Viktor Varga4Subcortical Modulation Research Group, Institute of Experimental Medicine, Budapest, HungarySubcortical Modulation Research Group, Institute of Experimental Medicine, Budapest, HungarySubcortical Modulation Research Group, Institute of Experimental Medicine, Budapest, HungaryLaboratory of Cerebral Cortex Research, Institute of Experimental Medicine, Budapest, HungarySubcortical Modulation Research Group, Institute of Experimental Medicine, Budapest, HungaryAscending serotonergic/glutamatergic projection from the median raphe region (MRR) to the hippocampal formation regulates both encoding and consolidation of memory and the oscillations associated with them. The firing of various types of MRR neurons exhibits rhythmic modulation coupled to hippocampal oscillatory activity. A possible intermediary between rhythm-generating forebrain regions and entrained ascending modulation may be the GABAergic circuit in the MRR, known to be targeted by a diverse array of top-down inputs. However, the activity of inhibitory MRR neurons in an awake animal is still largely unexplored. In this study, we utilized whole cell patch-clamp, single cell, and multichannel extracellular recordings of GABAergic and non-GABAergic MRR neurons in awake, head-fixed mice. First, we have demonstrated that glutamatergic and serotonergic neurons receive both transient, phasic, and sustained tonic inhibition. Then, we observed substantial heterogeneity of GABAergic firing patterns but a marked modulation of activity by brain states and fine timescale coupling of spiking to theta and ripple oscillations. We also uncovered a correlation between the preferred theta phase and the direction of activity change during ripples, suggesting the segregation of inhibitory neurons into functional groups. Finally, we could detect complementary alteration of non-GABAergic neurons’ ripple-coupled activity. Our findings support the assumption that the local inhibitory circuit in the MRR may synchronize ascending serotonergic/glutamatergic modulation with hippocampal activity on a subsecond timescale.https://www.frontiersin.org/articles/10.3389/fncir.2021.784034/fullGABAmedian raphein vivo awake patch-clamptheta oscillationhippocampal ripple
spellingShingle Marta Jelitai
Albert M. Barth
Ferenc Komlósi
Tamás F. Freund
Viktor Varga
Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
Frontiers in Neural Circuits
GABA
median raphe
in vivo awake patch-clamp
theta oscillation
hippocampal ripple
title Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
title_full Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
title_fullStr Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
title_full_unstemmed Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
title_short Activity and Coupling to Hippocampal Oscillations of Median Raphe GABAergic Cells in Awake Mice
title_sort activity and coupling to hippocampal oscillations of median raphe gabaergic cells in awake mice
topic GABA
median raphe
in vivo awake patch-clamp
theta oscillation
hippocampal ripple
url https://www.frontiersin.org/articles/10.3389/fncir.2021.784034/full
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