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

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          Abstract

          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.

          eLife digest

          To find their way around, animals – including humans – rely on an area of the brain called the hippocampus. Studies in rodents have shown that certain neurons in the hippocampus called place cells become active when an animal passes through specific locations. At each position, a different set of place cells fires. A journey from A to B will thus be accompanied by a sequential activation of place cells corresponding to a particular point.

          Rats can learn new routes to a given place. Every time they take a specific way, the connections between the activated place cells become stronger. After learning, the hippocampus replays the sequence of place cell activation both in the order the rat has experienced and backwards. This is known as reverse replay, which occurs more often when the animals find rewards at their destination. This suggests that reverse replay may help animals learn the routes to locations where food is available.

          To test this idea, Haga and Fukai built a computer model that simulates the hippocampal activity seen in a rat running through a maze. In contrast to previous models, which featured only forward replay, the new simulation also included reverse replay. The results confirmed that reverse replay helps the rodents to learn routes to rewarded locations. It also enables the hippocampus to combine multiple past experiences, which may teach animals that a combination of previous paths will lead to a reward, even if they have never tried the combined route before.

          The hippocampus has a central role in many different types of memory. The findings by Haga and Fukai may therefore provide a framework for studying the mechanisms of memory and decision-making. The results could even offer insight into the mechanisms of logical thinking. After all, the ability to combine multiple known paths into a new route bears some similarity to joining up thought processes such as ‘If Sophie oversleeps, she will miss the bus’ with ‘If Sophie misses the bus, she will be late for school’ to reason that ‘If Sophie oversleeps, she will be late for school’. Future studies should test whether reverse replay helps with this process of deduction.

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          Most cited references59

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          A model is presented that reproduces spiking and bursting behavior of known types of cortical neurons. The model combines the biologically plausibility of Hodgkin-Huxley-type dynamics and the computational efficiency of integrate-and-fire neurons. Using this model, one can simulate tens of thousands of spiking cortical neurons in real time (1 ms resolution) using a desktop PC.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                03 July 2018
                2018
                : 7
                : e34171
                Affiliations
                [1 ]RIKEN Center for Brain Science WakoJapan
                National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                Brown University United States
                National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                Author information
                http://orcid.org/0000-0003-3145-709X
                http://orcid.org/0000-0001-6977-5638
                Article
                34171
                10.7554/eLife.34171
                6059768
                29969098
                ee6e9361-0cee-42f0-8c47-c02726996ad5
                © 2018, Haga et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 07 December 2017
                : 02 July 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science, and Technology;
                Award ID: 15H04265
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003382, Core Research for Evolutional Science and Technology;
                Award ID: JPMJCR13W1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science, and Technology;
                Award ID: 16H01289
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science, and Technology;
                Award ID: 17H06036
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                The combination of short-term and long-term plasticity enables hippocampus to learn goal-directed paths through replay in a reversed order.

                Life sciences
                hippocampus,reverse replay,sequence learning,short-term plasticity,spike-timing-dependent plasticity,goal-directed learning,none

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