Binocular rivalry reveals an out-of-equilibrium neural dynamics suited for decision-making.

Levelt's propositions attractor dynamics binocular rivalry decision making discrete stochastic dominance distribution human neuroscience physics of living systems

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
09 08 2021
Historique:
received: 29 07 2020
accepted: 24 05 2021
entrez: 9 8 2021
pubmed: 10 8 2021
medline: 9 10 2021
Statut: epublish

Résumé

In ambiguous or conflicting sensory situations, perception is often 'multistable' in that it perpetually changes at irregular intervals, shifting abruptly between distinct alternatives. The interval statistics of these alternations exhibits quasi-universal characteristics, suggesting a general mechanism. Using binocular rivalry, we show that many aspects of this perceptual dynamics are reproduced by a hierarchical model operating out of equilibrium. The constitutive elements of this model idealize the metastability of cortical networks. Independent elements accumulate visual evidence at one level, while groups of coupled elements compete for dominance at another level. As soon as one group dominates perception, feedback inhibition suppresses supporting evidence. Previously unreported features in the serial dependencies of perceptual alternations compellingly corroborate this mechanism. Moreover, the proposed out-of-equilibrium dynamics satisfies normative constraints of continuous decision-making. Thus, multistable perception may reflect decision-making in a volatile world: integrating evidence over space and time, choosing categorically between hypotheses, while concurrently evaluating alternatives.

Identifiants

pubmed: 34369875
doi: 10.7554/eLife.61581
pii: 61581
pmc: PMC8352598
doi:
pii:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2021, Cao et al.

Déclaration de conflit d'intérêts

RC, AP, SA, JB none, MM None

Références

Neuron. 2009 Mar 12;61(5):750-61
pubmed: 19285471
Philos Trans R Soc Lond B Biol Sci. 1980 Jul 8;290(1038):181-97
pubmed: 6106237
Trends Neurosci. 2013 Mar;36(3):141-51
pubmed: 23273272
Atten Percept Psychophys. 2014 Feb;76(2):473-88
pubmed: 24178065
Curr Opin Neurobiol. 2019 Oct;58:37-45
pubmed: 31326722
J R Soc Interface. 2017 Nov;14(136):
pubmed: 29167370
PLoS Comput Biol. 2015 Jul 15;11(7):e1004196
pubmed: 26176664
J Opt Soc Am A Opt Image Sci Vis. 2009 Dec;26(12):2612-22
pubmed: 19956332
Sci Am. 1971 Dec;225(6):63-71
pubmed: 5116412
Cereb Cortex. 1997 Apr-May;7(3):237-52
pubmed: 9143444
J Chem Phys. 2018 Jan 7;148(1):010901
pubmed: 29306272
Annu Rev Vis Sci. 2020 Sep 15;6:387-409
pubmed: 32600168
PLoS One. 2015 Dec 15;10(12):e0144788
pubmed: 26671774
Trends Cogn Sci. 1999 Jul;3(7):254-264
pubmed: 10377540
Cereb Cortex. 2011 May;21(5):1118-33
pubmed: 20884721
Neuroimage. 2010 Sep;52(3):740-51
pubmed: 20083212
Atten Percept Psychophys. 2013 Feb;75(2):322-40
pubmed: 23150214
PLoS Comput Biol. 2013;9(3):e1002925
pubmed: 23516340
PLoS Comput Biol. 2020 Dec 14;16(12):e1008480
pubmed: 33315961
PLoS One. 2014 Sep 12;9(9):e107628
pubmed: 25216188
Annu Rev Neurosci. 2010;33:269-98
pubmed: 20345247
Atten Percept Psychophys. 2021 Aug;83(6):2613-2624
pubmed: 33890241
Trends Cogn Sci. 2018 Apr;22(4):294-306
pubmed: 29475638
J Neurosci. 2007 Oct 17;27(42):11192-200
pubmed: 17942714
J Vis. 2005 Apr 04;5(4):287-98
pubmed: 15929652
Perception. 1988;17(2):215-28
pubmed: 3067209
Nat Neurosci. 2008 Oct;11(10):1193-200
pubmed: 18711393
Proc Natl Acad Sci U S A. 2012 Jun 26;109 Suppl 1:10655-60
pubmed: 22723351
Curr Opin Neurobiol. 2016 Oct;40:14-22
pubmed: 27318972
Phys Rev Lett. 2014 Aug 29;113(9):098103
pubmed: 25216009
J Vis. 2008 May 23;8(5):12.1-19
pubmed: 18842083
J Neurosci. 2012 Aug 29;32(35):11956-69
pubmed: 22933781
Sci Rep. 2018 May 8;8(1):7106
pubmed: 29740086
Annu Rev Vis Sci. 2017 Sep 15;3:227-250
pubmed: 28715956
Nature. 2001 Aug 30;412(6850):907-10
pubmed: 11528478
J Vis. 2007 Jun 21;7(8):10
pubmed: 17685817
J Neurophysiol. 2007 Sep;98(3):1125-39
pubmed: 17615138
PLoS Comput Biol. 2017 Nov 20;13(11):e1005856
pubmed: 29155808
J Neurophysiol. 2011 Nov;106(5):2136-50
pubmed: 21775721
Nature. 1996 Feb 8;379(6565):549-53
pubmed: 8596635
Hum Neurobiol. 1985;4(4):219-27
pubmed: 3836989
Nat Rev Neurosci. 2010 Feb;11(2):127-38
pubmed: 20068583
Trends Cogn Sci. 2006 Jul;10(7):301-8
pubmed: 16784882
Vision Res. 2007 Sep;47(21):2741-50
pubmed: 17764714
Cereb Cortex. 2003 Apr;13(4):422-33
pubmed: 12631571
Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17507-12
pubmed: 17088545
Science. 2016 Dec 2;354(6316):1140-1144
pubmed: 27934763
J Vis. 2007 Jul 20;7(10):5.1-17
pubmed: 17997674
Nat Neurosci. 2010 Mar;13(3):369-78
pubmed: 20173745
Front Psychol. 2016 Nov 18;7:1792
pubmed: 27917138
Neuron. 2008 Dec 26;60(6):1142-52
pubmed: 19109917
Curr Opin Neurobiol. 2012 Dec;22(6):1039-46
pubmed: 23026743
Perception. 1985;14(2):135-43
pubmed: 4069943
PLoS Comput Biol. 2020 Aug 27;16(8):e1008152
pubmed: 32853256
Nat Neurosci. 1999 Jan;2(1):79-87
pubmed: 10195184
J Comput Neurosci. 2002 Jan-Feb;12(1):39-53
pubmed: 11932559
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14499-503
pubmed: 14612564
J Vis. 2008 Oct 29;8(13):7.1-14
pubmed: 19146337
Nat Neurosci. 2016 Dec;19(12):1682-1689
pubmed: 27643432
Vision Res. 2005 Mar;45(6):707-14
pubmed: 15639497
J Neurosci. 2016 Mar 16;36(11):3231-42
pubmed: 26985033
J Vis. 2019 Oct 1;19(12):15
pubmed: 31622474
Cognition. 2008 Sep;108(3):687-701
pubmed: 18649876
Nat Neurosci. 2012 Nov;15(11):1498-505
pubmed: 23001062
J Vis. 2006 Sep 21;6(10):1068-78
pubmed: 17132078
Vision Res. 1975 Jul;15(7):855-9
pubmed: 1154668
Vision Res. 2015 Apr;109(Pt A):20-37
pubmed: 25749677
Commun Biol. 2019 Aug 23;2:319
pubmed: 31453383
Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3408-13
pubmed: 9096407
Behav Brain Sci. 2001 Oct;24(5):793-810; discussion 810-48
pubmed: 12239890
Neuroreport. 2003 Jul 18;14(10):1347-52
pubmed: 12876471
Nature. 2015 May 28;521(7553):511-515
pubmed: 25849776
J Exp Psychol. 1971 Jun;88(3):327-32
pubmed: 5090924
Science. 1996 Dec 6;274(5293):1724-6
pubmed: 8939866
Neuron. 2012 Jun 7;74(5):924-35
pubmed: 22681695
Curr Biol. 2006 Jul 11;16(13):1351-7
pubmed: 16824924
Vision Res. 2006 Feb;46(3):392-406
pubmed: 16183099
J Neurosci. 1990 Dec;10(12):3880-8
pubmed: 2269889
Atten Percept Psychophys. 2016 Feb;78(2):674-84
pubmed: 26542402
PLoS One. 2007 Aug 15;2(8):e739
pubmed: 17710139
Psychol Rev. 2006 Oct;113(4):700-65
pubmed: 17014301
PLoS One. 2012;7(1):e30595
pubmed: 22295095
Front Comput Neurosci. 2016 Jun 14;10:56
pubmed: 27378899
Vision Res. 2005 Jan;45(1):29-40
pubmed: 15571736
Nature. 2004 Sep 30;431(7008):573-8
pubmed: 15457262
Kybernetik. 1972 Mar;10(3):139-44
pubmed: 5021011
Front Comput Neurosci. 2014 May 27;8:56
pubmed: 24904394
Neural Comput. 1998 Jul 1;10(5):1119-35
pubmed: 9654769
J Neurophysiol. 2003 Nov;90(5):3441-54
pubmed: 12773500
PLoS One. 2016 Jan 14;11(1):e0147454
pubmed: 26764910
Vis Neurosci. 1994 Jul-Aug;11(4):823-30
pubmed: 7918231
J Comput Neurosci. 2012 Apr;32(2):233-52
pubmed: 21748526
Nat Neurosci. 2018 Sep;21(9):1148-1160
pubmed: 30127428
Psychol Rev. 2004 Apr;111(2):333-67
pubmed: 15065913
Nat Rev Neurosci. 2011 Nov 23;13(1):51-62
pubmed: 22108672
Nat Neurosci. 2019 May;22(5):787-796
pubmed: 30936557
Philos Trans R Soc Lond B Biol Sci. 2009 May 12;364(1521):1235-43
pubmed: 19528004
Front Comput Neurosci. 2013 Mar 20;7:17
pubmed: 23518509
PLoS Comput Biol. 2012;8(3):e1002395
pubmed: 22479168
Nat Neurosci. 2017 Jan;20(1):107-114
pubmed: 27798630
Neuroimage. 2014 Oct 15;100:161-75
pubmed: 24945667
J Neurosci. 2010 Sep 15;30(37):12353-65
pubmed: 20844131
Atten Percept Psychophys. 2014 Jan;76(1):123-32
pubmed: 24097015
Nat Neurosci. 2013 Sep;16(9):1170-8
pubmed: 23955561
Curr Opin Neurobiol. 2017 Oct;46:31-38
pubmed: 28756341
Phys Rev E Stat Nonlin Soft Matter Phys. 2014 Dec;90(6):062710
pubmed: 25615132
PLoS Comput Biol. 2009 Jul;5(7):e1000430
pubmed: 19593372
J Neurosci. 2015 May 27;35(21):8214-31
pubmed: 26019337
Philos Trans R Soc Lond B Biol Sci. 1998 Nov 29;353(1377):1801-18
pubmed: 9854253
Vis Neurosci. 1992 May;8(5):469-78
pubmed: 1586647
J Vis. 2006 Oct 26;6(11):1244-56
pubmed: 17209732
Nature. 1996 Apr 18;380(6575):621-4
pubmed: 8602261
Nature. 2016 Apr 21;532(7599):370-4
pubmed: 27018655
Perception. 1977;6(6):645-56
pubmed: 600664
J Neurosci. 2016 Jun 29;36(26):6957-72
pubmed: 27358454
J Opt Soc Am A Opt Image Sci Vis. 2003 Jul;20(7):1434-48
pubmed: 12868647
Trends Cogn Sci. 2007 Mar;11(3):118-25
pubmed: 17276130
J Vis. 2010 Sep 01;10(11):1
pubmed: 20884496
Nature. 1974 May 31;249(456):488-90
pubmed: 4834239
Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15508-11
pubmed: 8986842
Philos Trans R Soc Lond B Biol Sci. 2012 Apr 5;367(1591):1001-12
pubmed: 22371621
Curr Biol. 2003 Jul 1;13(13):1076-85
pubmed: 12842006
J Neurophysiol. 2015 Jan 1;113(1):277-94
pubmed: 25343785
Curr Opin Neurobiol. 2008 Apr;18(2):217-22
pubmed: 18678253
Vis Neurosci. 2015 Jan;32:E020
pubmed: 26241699
J Vis. 2009 Jan 15;9(1):17.1-11
pubmed: 19271887
Annu Rev Neurosci. 2000;23:315-41
pubmed: 10845067
Prog Neurobiol. 2005 Jul;76(4):236-56
pubmed: 16257103
Front Neurosci. 2014 Feb 28;8:25
pubmed: 24616656
Neuron. 2009 Jan 29;61(2):168-85
pubmed: 19186161
Nat Neurosci. 2006 Nov;9(11):1432-8
pubmed: 17057707
J Comput Neurosci. 2009 Aug;27(1):37-54
pubmed: 19125318
Proc Natl Acad Sci U S A. 2017 Jul 25;114(30):E6192-E6201
pubmed: 28696323
PLoS Comput Biol. 2017 May 15;13(5):e1005536
pubmed: 28505152
Nat Neurosci. 2002 Jun;5(6):605-9
pubmed: 11992115
Cell Rep. 2019 Jun 4;27(10):2909-2920.e4
pubmed: 31167137
Nat Rev Neurosci. 2002 Jan;3(1):13-21
pubmed: 11823801
Annu Rev Neurosci. 2007;30:535-74
pubmed: 17600525
Vision Res. 2001 Apr;41(8):981-9
pubmed: 11301073
Nature. 2015 Feb 19;518(7539):399-403
pubmed: 25652823
Philos Trans R Soc Lond B Biol Sci. 2012 Apr 5;367(1591):896-905
pubmed: 22371612
J Neurosci. 2019 Aug 7;39(32):6265-6275
pubmed: 31182633
Neuron. 2008 Oct 23;60(2):215-34
pubmed: 18957215
Curr Opin Behav Sci. 2018 Oct;11:100-108
pubmed: 30175197
Atten Percept Psychophys. 2013 Aug;75(6):1215-29
pubmed: 23673611
Vision Res. 1978;18(7):827-35
pubmed: 676090
J Neurosci. 2013 Jul 3;33(27):11155-68
pubmed: 23825419
Neuropsychologia. 2017 Sep;104:92-101
pubmed: 28782543
Nat Neurosci. 2003 Aug;6(8):891-8
pubmed: 12858179
Science. 1972 Aug 18;177(4049):567-75
pubmed: 4626069
Anat Embryol (Berl). 1994 Oct;190(4):307-37
pubmed: 7840420
J Neurosci. 2016 Apr 06;36(14):4121-35
pubmed: 27053217
Neuron. 2002 Dec 5;36(5):955-68
pubmed: 12467598
Nat Neurosci. 2016 Jul;19(7):973-80
pubmed: 27273768

Auteurs

Robin Cao (R)

Cognitive Biology, Center for Behavioral Brain Sciences, Magdeburg, Germany.
Gatsby Computational Neuroscience Unit, London, United Kingdom.
Istituto Superiore di Sanità, Rome, Italy.

Alexander Pastukhov (A)

Cognitive Biology, Center for Behavioral Brain Sciences, Magdeburg, Germany.

Stepan Aleshin (S)

Cognitive Biology, Center for Behavioral Brain Sciences, Magdeburg, Germany.

Maurizio Mattia (M)

Istituto Superiore di Sanità, Rome, Italy.

Jochen Braun (J)

Cognitive Biology, Center for Behavioral Brain Sciences, Magdeburg, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH