Active hippocampal networks undergo spontaneous synaptic modification.

The brain is self-writable; as the brain voluntarily adapts itself to a changing environment, the neural circuitry rearranges its functional connectivity by referring to its own activity. How the internal activity modifies synaptic weights is largely unknown, however. Here we report that spontaneous...

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Main Authors: Masako Tsukamoto-Yasui, Takuya Sasaki, Wataru Matsumoto, Ayako Hasegawa, Takeshi Toyoda, Atsushi Usami, Yuichi Kubota, Taku Ochiai, Tomokatsu Hori, Norio Matsuki, Yuji Ikegaya
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2082078?pdf=render
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spelling doaj-ad40ad7fdb76404cbd1944879aa55bed2020-11-25T01:46:01ZengPublic Library of Science (PLoS)PLoS ONE1932-62032007-01-01211e125010.1371/journal.pone.0001250Active hippocampal networks undergo spontaneous synaptic modification.Masako Tsukamoto-YasuiTakuya SasakiWataru MatsumotoAyako HasegawaTakeshi ToyodaAtsushi UsamiYuichi KubotaTaku OchiaiTomokatsu HoriNorio MatsukiYuji IkegayaThe brain is self-writable; as the brain voluntarily adapts itself to a changing environment, the neural circuitry rearranges its functional connectivity by referring to its own activity. How the internal activity modifies synaptic weights is largely unknown, however. Here we report that spontaneous activity causes complex reorganization of synaptic connectivity without any external (or artificial) stimuli. Under physiologically relevant ionic conditions, CA3 pyramidal cells in hippocampal slices displayed spontaneous spikes with bistable slow oscillations of membrane potential, alternating between the so-called UP and DOWN states. The generation of slow oscillations did not require fast synaptic transmission, but their patterns were coordinated by local circuit activity. In the course of generating spontaneous activity, individual neurons acquired bidirectional long-lasting synaptic modification. The spontaneous synaptic plasticity depended on a rise in intracellular calcium concentrations of postsynaptic cells, but not on NMDA receptor activity. The direction and amount of the plasticity varied depending on slow oscillation patterns and synapse locations, and thus, they were diverse in a network. Once this global synaptic refinement occurred, the same neurons now displayed different patterns of spontaneous activity, which in turn exhibited different levels of synaptic plasticity. Thus, active networks continuously update their internal states through ongoing synaptic plasticity. With computational simulations, we suggest that with this slow oscillation-induced plasticity, a recurrent network converges on a more specific state, compared to that with spike timing-dependent plasticity alone.http://europepmc.org/articles/PMC2082078?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Masako Tsukamoto-Yasui
Takuya Sasaki
Wataru Matsumoto
Ayako Hasegawa
Takeshi Toyoda
Atsushi Usami
Yuichi Kubota
Taku Ochiai
Tomokatsu Hori
Norio Matsuki
Yuji Ikegaya
spellingShingle Masako Tsukamoto-Yasui
Takuya Sasaki
Wataru Matsumoto
Ayako Hasegawa
Takeshi Toyoda
Atsushi Usami
Yuichi Kubota
Taku Ochiai
Tomokatsu Hori
Norio Matsuki
Yuji Ikegaya
Active hippocampal networks undergo spontaneous synaptic modification.
PLoS ONE
author_facet Masako Tsukamoto-Yasui
Takuya Sasaki
Wataru Matsumoto
Ayako Hasegawa
Takeshi Toyoda
Atsushi Usami
Yuichi Kubota
Taku Ochiai
Tomokatsu Hori
Norio Matsuki
Yuji Ikegaya
author_sort Masako Tsukamoto-Yasui
title Active hippocampal networks undergo spontaneous synaptic modification.
title_short Active hippocampal networks undergo spontaneous synaptic modification.
title_full Active hippocampal networks undergo spontaneous synaptic modification.
title_fullStr Active hippocampal networks undergo spontaneous synaptic modification.
title_full_unstemmed Active hippocampal networks undergo spontaneous synaptic modification.
title_sort active hippocampal networks undergo spontaneous synaptic modification.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2007-01-01
description The brain is self-writable; as the brain voluntarily adapts itself to a changing environment, the neural circuitry rearranges its functional connectivity by referring to its own activity. How the internal activity modifies synaptic weights is largely unknown, however. Here we report that spontaneous activity causes complex reorganization of synaptic connectivity without any external (or artificial) stimuli. Under physiologically relevant ionic conditions, CA3 pyramidal cells in hippocampal slices displayed spontaneous spikes with bistable slow oscillations of membrane potential, alternating between the so-called UP and DOWN states. The generation of slow oscillations did not require fast synaptic transmission, but their patterns were coordinated by local circuit activity. In the course of generating spontaneous activity, individual neurons acquired bidirectional long-lasting synaptic modification. The spontaneous synaptic plasticity depended on a rise in intracellular calcium concentrations of postsynaptic cells, but not on NMDA receptor activity. The direction and amount of the plasticity varied depending on slow oscillation patterns and synapse locations, and thus, they were diverse in a network. Once this global synaptic refinement occurred, the same neurons now displayed different patterns of spontaneous activity, which in turn exhibited different levels of synaptic plasticity. Thus, active networks continuously update their internal states through ongoing synaptic plasticity. With computational simulations, we suggest that with this slow oscillation-induced plasticity, a recurrent network converges on a more specific state, compared to that with spike timing-dependent plasticity alone.
url http://europepmc.org/articles/PMC2082078?pdf=render
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