Recurrent network model for learning goal-directed sequences through reverse replay

Reverse replay of hippocampal place cells occurs frequently at rewarded locations, suggesting its contribution to goal-directed path learning. Symmetric spike-timing dependent plasticity (STDP) in CA3 likely potentiates recurrent synapses for both forward (start to goal) and reverse (goal to start)...

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Main Authors: Tatsuya Haga, Tomoki Fukai
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/34171
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author Tatsuya Haga
Tomoki Fukai
author_facet Tatsuya Haga
Tomoki Fukai
author_sort Tatsuya Haga
collection DOAJ
description Reverse replay of hippocampal place cells occurs frequently at rewarded locations, suggesting its contribution to goal-directed path learning. Symmetric spike-timing dependent plasticity (STDP) in CA3 likely potentiates recurrent synapses for both forward (start to goal) and reverse (goal to start) replays during sequential activation of place cells. However, how reverse replay selectively strengthens forward synaptic pathway is unclear. Here, we show computationally that firing sequences bias synaptic transmissions to the opposite direction of propagation under symmetric STDP in the co-presence of short-term synaptic depression or afterdepolarization. We demonstrate that significant biases are created in biologically realistic simulation settings, and this bias enables reverse replay to enhance goal-directed spatial memory on a W-maze. Further, we show that essentially the same mechanism works in a two-dimensional open field. Our model for the first time provides the mechanistic account for the way reverse replay contributes to hippocampal sequence learning for reward-seeking spatial navigation.
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spelling doaj.art-1df2b2200efb4c51840d691b7fc4f9a82022-12-22T03:33:51ZengeLife Sciences Publications LtdeLife2050-084X2018-07-01710.7554/eLife.34171Recurrent network model for learning goal-directed sequences through reverse replayTatsuya Haga0https://orcid.org/0000-0003-3145-709XTomoki Fukai1https://orcid.org/0000-0001-6977-5638RIKEN Center for Brain Science, Wako, JapanRIKEN Center for Brain Science, Wako, JapanReverse replay of hippocampal place cells occurs frequently at rewarded locations, suggesting its contribution to goal-directed path learning. Symmetric spike-timing dependent plasticity (STDP) in CA3 likely potentiates recurrent synapses for both forward (start to goal) and reverse (goal to start) replays during sequential activation of place cells. However, how reverse replay selectively strengthens forward synaptic pathway is unclear. Here, we show computationally that firing sequences bias synaptic transmissions to the opposite direction of propagation under symmetric STDP in the co-presence of short-term synaptic depression or afterdepolarization. We demonstrate that significant biases are created in biologically realistic simulation settings, and this bias enables reverse replay to enhance goal-directed spatial memory on a W-maze. Further, we show that essentially the same mechanism works in a two-dimensional open field. Our model for the first time provides the mechanistic account for the way reverse replay contributes to hippocampal sequence learning for reward-seeking spatial navigation.https://elifesciences.org/articles/34171hippocampusreverse replaysequence learningshort-term plasticityspike-timing-dependent plasticitygoal-directed learning
spellingShingle Tatsuya Haga
Tomoki Fukai
Recurrent network model for learning goal-directed sequences through reverse replay
eLife
hippocampus
reverse replay
sequence learning
short-term plasticity
spike-timing-dependent plasticity
goal-directed learning
title Recurrent network model for learning goal-directed sequences through reverse replay
title_full Recurrent network model for learning goal-directed sequences through reverse replay
title_fullStr Recurrent network model for learning goal-directed sequences through reverse replay
title_full_unstemmed Recurrent network model for learning goal-directed sequences through reverse replay
title_short Recurrent network model for learning goal-directed sequences through reverse replay
title_sort recurrent network model for learning goal directed sequences through reverse replay
topic hippocampus
reverse replay
sequence learning
short-term plasticity
spike-timing-dependent plasticity
goal-directed learning
url https://elifesciences.org/articles/34171
work_keys_str_mv AT tatsuyahaga recurrentnetworkmodelforlearninggoaldirectedsequencesthroughreversereplay
AT tomokifukai recurrentnetworkmodelforlearninggoaldirectedsequencesthroughreversereplay