Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake Replay

Jun Yamamoto, Susumu Tonegawa

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

Hippocampal replays have been demonstrated to play a crucial role in memory. Chains of ripples (ripple bursts) in CA1 have been reported to co-occur with long-range place cell sequence replays during the quiet awake state, but roles of neural inputs to CA1 in ripple bursts and replays are unknown. Here we show that ripple bursts in CA1 and medial entorhinal cortex (MEC) are temporally associated. An inhibition of MECIII input to CA1 during quiet awake reduced ripple bursts in CA1 and restricted the spatial coverage of replays to a shorter distance corresponding to single ripple events. The reduction did not occur with MECIII input inhibition during slow-wave sleep. Inhibition of CA3 activity suppressed ripples and replays in CA1 regardless of behavioral state. Thus, MECIII input to CA1 is crucial for ripple bursts and long-range replays specifically in quiet awake, whereas CA3 input is essential for both, regardless of behavioral state. Yamamoto and Tonegawa aim to determine the contribution of MECIII and CA3 inputs to hippocampal ripples and replays. They found differential roles of MECIII and CA3 inputs on CA1 ripples and replays during animal's different behavioral states.

Original languageEnglish (US)
Pages (from-to)217-227.e4
JournalNeuron
Volume96
Issue number1
DOIs
StatePublished - Sep 27 2017

Fingerprint

Entorhinal Cortex
Sleep
Inhibition (Psychology)

Keywords

  • awake
  • decoding
  • entorhinal cortex
  • hippocampus
  • optogenetics
  • replay
  • sharp-wave ripple
  • single-unit recording
  • slow-wave sleep
  • transgenic mice

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake Replay. / Yamamoto, Jun; Tonegawa, Susumu.

In: Neuron, Vol. 96, No. 1, 27.09.2017, p. 217-227.e4.

Research output: Contribution to journalArticle

@article{aa84a438d80d459ea0cbd44a84899eab,
title = "Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake Replay",
abstract = "Hippocampal replays have been demonstrated to play a crucial role in memory. Chains of ripples (ripple bursts) in CA1 have been reported to co-occur with long-range place cell sequence replays during the quiet awake state, but roles of neural inputs to CA1 in ripple bursts and replays are unknown. Here we show that ripple bursts in CA1 and medial entorhinal cortex (MEC) are temporally associated. An inhibition of MECIII input to CA1 during quiet awake reduced ripple bursts in CA1 and restricted the spatial coverage of replays to a shorter distance corresponding to single ripple events. The reduction did not occur with MECIII input inhibition during slow-wave sleep. Inhibition of CA3 activity suppressed ripples and replays in CA1 regardless of behavioral state. Thus, MECIII input to CA1 is crucial for ripple bursts and long-range replays specifically in quiet awake, whereas CA3 input is essential for both, regardless of behavioral state. Yamamoto and Tonegawa aim to determine the contribution of MECIII and CA3 inputs to hippocampal ripples and replays. They found differential roles of MECIII and CA3 inputs on CA1 ripples and replays during animal's different behavioral states.",
keywords = "awake, decoding, entorhinal cortex, hippocampus, optogenetics, replay, sharp-wave ripple, single-unit recording, slow-wave sleep, transgenic mice",
author = "Jun Yamamoto and Susumu Tonegawa",
year = "2017",
month = "9",
day = "27",
doi = "10.1016/j.neuron.2017.09.017",
language = "English (US)",
volume = "96",
pages = "217--227.e4",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",
number = "1",

}

TY - JOUR

T1 - Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake Replay

AU - Yamamoto, Jun

AU - Tonegawa, Susumu

PY - 2017/9/27

Y1 - 2017/9/27

N2 - Hippocampal replays have been demonstrated to play a crucial role in memory. Chains of ripples (ripple bursts) in CA1 have been reported to co-occur with long-range place cell sequence replays during the quiet awake state, but roles of neural inputs to CA1 in ripple bursts and replays are unknown. Here we show that ripple bursts in CA1 and medial entorhinal cortex (MEC) are temporally associated. An inhibition of MECIII input to CA1 during quiet awake reduced ripple bursts in CA1 and restricted the spatial coverage of replays to a shorter distance corresponding to single ripple events. The reduction did not occur with MECIII input inhibition during slow-wave sleep. Inhibition of CA3 activity suppressed ripples and replays in CA1 regardless of behavioral state. Thus, MECIII input to CA1 is crucial for ripple bursts and long-range replays specifically in quiet awake, whereas CA3 input is essential for both, regardless of behavioral state. Yamamoto and Tonegawa aim to determine the contribution of MECIII and CA3 inputs to hippocampal ripples and replays. They found differential roles of MECIII and CA3 inputs on CA1 ripples and replays during animal's different behavioral states.

AB - Hippocampal replays have been demonstrated to play a crucial role in memory. Chains of ripples (ripple bursts) in CA1 have been reported to co-occur with long-range place cell sequence replays during the quiet awake state, but roles of neural inputs to CA1 in ripple bursts and replays are unknown. Here we show that ripple bursts in CA1 and medial entorhinal cortex (MEC) are temporally associated. An inhibition of MECIII input to CA1 during quiet awake reduced ripple bursts in CA1 and restricted the spatial coverage of replays to a shorter distance corresponding to single ripple events. The reduction did not occur with MECIII input inhibition during slow-wave sleep. Inhibition of CA3 activity suppressed ripples and replays in CA1 regardless of behavioral state. Thus, MECIII input to CA1 is crucial for ripple bursts and long-range replays specifically in quiet awake, whereas CA3 input is essential for both, regardless of behavioral state. Yamamoto and Tonegawa aim to determine the contribution of MECIII and CA3 inputs to hippocampal ripples and replays. They found differential roles of MECIII and CA3 inputs on CA1 ripples and replays during animal's different behavioral states.

KW - awake

KW - decoding

KW - entorhinal cortex

KW - hippocampus

KW - optogenetics

KW - replay

KW - sharp-wave ripple

KW - single-unit recording

KW - slow-wave sleep

KW - transgenic mice

UR - http://www.scopus.com/inward/record.url?scp=85031045202&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85031045202&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2017.09.017

DO - 10.1016/j.neuron.2017.09.017

M3 - Article

VL - 96

SP - 217-227.e4

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 1

ER -