Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation
Name:
journal.pcbi.1006624.pdf
Size:
3.436Mb
Format:
PDF
Description:
Final Published Version
Author
Cazin, NicolasLlofriu Alonso, Martin
Scleidorovich Chiodi, Pablo
Pelc, Tatiana
Harland, Bruce
Weitzenfeld, Alfredo
Fellous, Jean-Marc
Dominey, Peter Ford
Affiliation
Univ Arizona, Dept PsycholIssue Date
2019-07-15
Metadata
Show full item recordPublisher
PUBLIC LIBRARY SCIENCECitation
Cazin N, Llofriu Alonso M, Scleidorovich Chiodi P, Pelc T, Harland B, Weitzenfeld A, et al. (2019) Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation. PLoS Comput Biol 15(7): e1006624. https://doi.org/10.1371/journal.pcbi.1006624Journal
PLOS COMPUTATIONAL BIOLOGYRights
Copyright © 2019 Cazin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Collection Information
This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.Abstract
As rats learn to search for multiple sources of food or water in a complex environment, they generate increasingly efficient trajectories between reward sites. Such spatial navigation capacity involves the replay of hippocampal place-cells during awake states, generating small sequences of spatially related place-cell activity that we call "snippets". These snippets occur primarily during sharp-wave-ripples (SWRs). Here we focus on the role of such replay events, as the animal is learning a traveling salesperson task (TSP) across multiple trials. We hypothesize that snippet replay generates synthetic data that can substantially expand and restructure the experience available and make learning more optimal. We developed a model of snippet generation that is modulated by reward, propagated in the forward and reverse directions. This implements a form of spatial credit assignment for reinforcement learning. We use a biologically motivated computational framework known as 'reservoir computing' to model prefrontal cortex (PFC) in sequence learning, in which large pools of prewired neural elements process information dynamically through reverberations. This PFC model consolidates snippets into larger spatial sequences that may be later recalled by subsets of the original sequences. Our simulation experiments provide neurophysiological explanations for two pertinent observations related to navigation. Reward modulation allows the system to reject non-optimal segments of experienced trajectories, and reverse replay allows the system to "learn" trajectories that it has not physically experienced, both of which significantly contribute to the TSP behavior.Note
Open access journalISSN
1553-7358PubMed ID
31306421Version
Final published versionSponsors
CRCNS NFS-ANR [1429929]ae974a485f413a2113503eed53cd6c53
10.1371/journal.pcbi.1006624
Scopus Count
Collections
Related articles
- Real-time sensory-motor integration of hippocampal place cell replay and prefrontal sequence learning in simulated and physical rat robots for novel path optimization.
- Authors: Cazin N, Scleidorovich P, Weitzenfeld A, Dominey PF
- Issue date: 2020 Apr
- Hippocampal-Prefrontal Reactivation during Learning Is Stronger in Awake Compared with Sleep States.
- Authors: Tang W, Shin JD, Frank LM, Jadhav SP
- Issue date: 2017 Dec 6
- Dynamics of Awake Hippocampal-Prefrontal Replay for Spatial Learning and Memory-Guided Decision Making.
- Authors: Shin JD, Tang W, Jadhav SP
- Issue date: 2019 Dec 18
- A model for navigation in unknown environments based on a reservoir of hippocampal sequences.
- Authors: Leibold C
- Issue date: 2020 Apr
- Reverse Replay of Hippocampal Place Cells Is Uniquely Modulated by Changing Reward.
- Authors: Ambrose RE, Pfeiffer BE, Foster DJ
- Issue date: 2016 Sep 7