Understanding the computation of time using neural network models.

interval timing neural network model population coding

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
12 05 2020
Historique:
pubmed: 29 4 2020
medline: 29 4 2020
entrez: 29 4 2020
Statut: ppublish

Résumé

To maximize future rewards in this ever-changing world, animals must be able to discover the temporal structure of stimuli and then anticipate or act correctly at the right time. How do animals perceive, maintain, and use time intervals ranging from hundreds of milliseconds to multiseconds in working memory? How is temporal information processed concurrently with spatial information and decision making? Why are there strong neuronal temporal signals in tasks in which temporal information is not required? A systematic understanding of the underlying neural mechanisms is still lacking. Here, we addressed these problems using supervised training of recurrent neural network models. We revealed that neural networks perceive elapsed time through state evolution along stereotypical trajectory, maintain time intervals in working memory in the monotonic increase or decrease of the firing rates of interval-tuned neurons, and compare or produce time intervals by scaling state evolution speed. Temporal and nontemporal information is coded in subspaces orthogonal with each other, and the state trajectories with time at different nontemporal information are quasiparallel and isomorphic. Such coding geometry facilitates the decoding generalizability of temporal and nontemporal information across each other. The network structure exhibits multiple feedforward sequences that mutually excite or inhibit depending on whether their preferences of nontemporal information are similar or not. We identified four factors that facilitate strong temporal signals in nontiming tasks, including the anticipation of coming events. Our work discloses fundamental computational principles of temporal processing, and it is supported by and gives predictions to a number of experimental phenomena.

Identifiants

pubmed: 32341153
pii: 1921609117
doi: 10.1073/pnas.1921609117
pmc: PMC7229760
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10530-10540

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

Références

Elife. 2016 Apr 12;5:
pubmed: 27067378
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13339-44
pubmed: 8917592
Psychol Monogr. 1963;77(13):1-31
pubmed: 5877542
Elife. 2018 Mar 14;7:
pubmed: 29537963
Brain Res Cogn Brain Res. 2004 Oct;21(2):139-70
pubmed: 15464348
J Neurosci. 2010 Jan 6;30(1):350-60
pubmed: 20053916
J Neurosci. 2010 Jul 14;30(28):9424-30
pubmed: 20631171
Nature. 2002 Sep 5;419(6902):65-70
pubmed: 12214232
Neuron. 2002 Dec 5;36(5):955-68
pubmed: 12467598
Trends Cogn Sci. 2008 Jul;12(7):273-80
pubmed: 18539519
Neuron. 2007 Feb 1;53(3):427-38
pubmed: 17270738
Trends Cogn Sci. 2018 Oct;22(10):911-922
pubmed: 30266150
Neural Comput. 2018 Feb;30(2):378-396
pubmed: 29162002
Neuron. 2003 Apr 24;38(2):317-27
pubmed: 12718864
Annu Rev Neurosci. 2013 Jul 8;36:313-36
pubmed: 23725000
Nat Neurosci. 2018 Jan;21(1):102-110
pubmed: 29203897
Proc Natl Acad Sci U S A. 2019 Apr 9;116(15):7523-7532
pubmed: 30918128
Neuron. 2018 Jun 6;98(5):1005-1019.e5
pubmed: 29879384
Neuron. 2016 Apr 6;90(1):128-42
pubmed: 26971945
Front Syst Neurosci. 2015 Dec 18;9:173
pubmed: 26733825
J Neurosci. 2014 May 14;34(20):6790-806
pubmed: 24828633
Nat Neurosci. 2017 Aug 29;20(9):1199-1208
pubmed: 28849791
Nature. 2013 Nov 7;503(7474):78-84
pubmed: 24201281
Nat Neurosci. 2019 Feb;22(2):297-306
pubmed: 30643294
Neuron. 2016 May 18;90(4):877-92
pubmed: 27196977
Annu Rev Neurosci. 2011;34:89-103
pubmed: 21438687
Nat Neurosci. 2016 Apr;19(4):613-22
pubmed: 26900926
Neuron. 2013 Apr 24;78(2):364-75
pubmed: 23562541
Nature. 2012 Jul 5;487(7405):51-6
pubmed: 22722855
Nat Commun. 2018 Mar 15;9(1):1098
pubmed: 29545587
Curr Biol. 2012 Nov 20;22(22):2095-103
pubmed: 23084992
J Neurosci. 2000 Feb 1;20(3):1129-41
pubmed: 10648718
J Neurosci. 2013 May 22;33(21):9082-96
pubmed: 23699519
Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):19156-61
pubmed: 19850874
Annu Rev Neurosci. 2004;27:307-40
pubmed: 15217335
J Neurosci. 2014 Mar 12;34(11):3910-23
pubmed: 24623769
Nat Neurosci. 2015 Jul;18(7):1025-33
pubmed: 26075643
Nat Neurosci. 2009 Apr;12(4):502-7
pubmed: 19252498
PLoS Biol. 2009 Jul;7(7):e1000141
pubmed: 19582146
Nat Neurosci. 2019 Feb;22(2):275-283
pubmed: 30664767
PLoS Biol. 2019 Apr 8;17(4):e3000054
pubmed: 30958818
Psychol Rev. 1988 Apr;95(2):274-95
pubmed: 3375401
Annu Rev Psychol. 2014;65:743-71
pubmed: 24050187
Cereb Cortex. 1994 Nov-Dec;4(6):590-600
pubmed: 7703686
J Neurosci. 2018 Apr 25;38(17):4186-4199
pubmed: 29615484
Proc Natl Acad Sci U S A. 2019 May 14;116(20):10097-10102
pubmed: 31028148
J Neurosci. 2011 Mar 9;31(10):3805-12
pubmed: 21389235
Annu Rev Neurosci. 2007;30:535-74
pubmed: 17600525
Proc Natl Acad Sci U S A. 2017 Jan 10;114(2):394-399
pubmed: 28028221
Front Psychol. 2014 Nov 19;5:1329
pubmed: 25477849
Nat Rev Neurosci. 2005 Oct;6(10):755-65
pubmed: 16163383
PLoS Comput Biol. 2016 Feb 29;12(2):e1004792
pubmed: 26928718
Neuron. 2018 May 16;98(4):687-705
pubmed: 29772201
Nat Neurosci. 2019 Jul;22(7):1159-1167
pubmed: 31182866
Nature. 1999 Jun 3;399(6735):470-3
pubmed: 10365959

Auteurs

Zedong Bi (Z)

Institute for Future, Qingdao University, Shandong 266071, China.
Department of Physics, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China.
Centre for Nonlinear Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China.
Institute of Computational and Theoretical Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China.
Research Centre, Hong Kong Baptist University Institute of Research and Continuing Education, Shenzhen 51800, China.

Changsong Zhou (C)

Department of Physics, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China; cszhou@hkbu.edu.hk.
Centre for Nonlinear Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China.
Institute of Computational and Theoretical Studies, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China.
Research Centre, Hong Kong Baptist University Institute of Research and Continuing Education, Shenzhen 51800, China.
Beijing Computational Science Research Center, Beijing 100193, China.
Department of Physics, Zhejiang University, Hangzhou 310027, China.

Classifications MeSH