Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

The hippocampus is critical for memory formation. The hypothalamic supramammillary nucleus (SuM) sends long-range projections to hippocampal area CA2. While the SuM-CA2 connection is critical for social memory, how this input acts on the local circuit is unknown. Using transgenic mice, we found that...

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Main Authors: Vincent Robert, Ludivine Therreau, Vivien Chevaleyre, Eude Lepicard, Cécile Viollet, Julie Cognet, Arthur JY Huang, Roman Boehringer, Denis Polygalov, Thomas J McHugh, Rebecca Ann Piskorowski
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/63352
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author Vincent Robert
Ludivine Therreau
Vivien Chevaleyre
Eude Lepicard
Cécile Viollet
Julie Cognet
Arthur JY Huang
Roman Boehringer
Denis Polygalov
Thomas J McHugh
Rebecca Ann Piskorowski
author_facet Vincent Robert
Ludivine Therreau
Vivien Chevaleyre
Eude Lepicard
Cécile Viollet
Julie Cognet
Arthur JY Huang
Roman Boehringer
Denis Polygalov
Thomas J McHugh
Rebecca Ann Piskorowski
author_sort Vincent Robert
collection DOAJ
description The hippocampus is critical for memory formation. The hypothalamic supramammillary nucleus (SuM) sends long-range projections to hippocampal area CA2. While the SuM-CA2 connection is critical for social memory, how this input acts on the local circuit is unknown. Using transgenic mice, we found that SuM axon stimulation elicited mixed excitatory and inhibitory responses in area CA2 pyramidal neurons (PNs). Parvalbumin-expressing basket cells were largely responsible for the feedforward inhibitory drive of SuM over area CA2. Inhibition recruited by the SuM input onto CA2 PNs increased the precision of action potential firing both in conditions of low and high cholinergic tone. Furthermore, SuM stimulation in area CA2 modulated CA1 activity, indicating that synchronized CA2 output drives a pulsed inhibition in area CA1. Hence, the network revealed here lays basis for understanding how SuM activity directly acts on the local hippocampal circuit to allow social memory encoding.
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spelling doaj.art-b29f3861e1344093a79123b0364004b82022-12-22T03:37:50ZengeLife Sciences Publications LtdeLife2050-084X2021-05-011010.7554/eLife.63352Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1Vincent Robert0Ludivine Therreau1Vivien Chevaleyre2Eude Lepicard3Cécile Viollet4Julie Cognet5Arthur JY Huang6Roman Boehringer7https://orcid.org/0000-0003-2856-3262Denis Polygalov8https://orcid.org/0000-0002-8165-5257Thomas J McHugh9https://orcid.org/0000-0002-1243-5189Rebecca Ann Piskorowski10https://orcid.org/0000-0003-0120-2360INSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, FranceINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, FranceINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, France; GHU Paris Psychiatrie and Neurosciences, Paris, FranceINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, FranceINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, FranceINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, FranceLaboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Saitama, JapanLaboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Saitama, JapanLaboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Saitama, JapanLaboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Saitama, JapanINSERM UMR1266, Institute of Psychiatry and Neuroscience of Paris, Team Synaptic Plasticity and Neural Networks, Université de Paris, Paris, France; GHU Paris Psychiatrie and Neurosciences, Paris, FranceThe hippocampus is critical for memory formation. The hypothalamic supramammillary nucleus (SuM) sends long-range projections to hippocampal area CA2. While the SuM-CA2 connection is critical for social memory, how this input acts on the local circuit is unknown. Using transgenic mice, we found that SuM axon stimulation elicited mixed excitatory and inhibitory responses in area CA2 pyramidal neurons (PNs). Parvalbumin-expressing basket cells were largely responsible for the feedforward inhibitory drive of SuM over area CA2. Inhibition recruited by the SuM input onto CA2 PNs increased the precision of action potential firing both in conditions of low and high cholinergic tone. Furthermore, SuM stimulation in area CA2 modulated CA1 activity, indicating that synchronized CA2 output drives a pulsed inhibition in area CA1. Hence, the network revealed here lays basis for understanding how SuM activity directly acts on the local hippocampal circuit to allow social memory encoding.https://elifesciences.org/articles/63352hippocampussupramammillary nucleusarea CA2hippocampal circuitryinhibitionsocial memory
spellingShingle Vincent Robert
Ludivine Therreau
Vivien Chevaleyre
Eude Lepicard
Cécile Viollet
Julie Cognet
Arthur JY Huang
Roman Boehringer
Denis Polygalov
Thomas J McHugh
Rebecca Ann Piskorowski
Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
eLife
hippocampus
supramammillary nucleus
area CA2
hippocampal circuitry
inhibition
social memory
title Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
title_full Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
title_fullStr Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
title_full_unstemmed Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
title_short Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
title_sort local circuit allowing hypothalamic control of hippocampal area ca2 activity and consequences for ca1
topic hippocampus
supramammillary nucleus
area CA2
hippocampal circuitry
inhibition
social memory
url https://elifesciences.org/articles/63352
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