Decoding rapidly presented visual stimuli from prefrontal ensembles without report nor post-perceptual processing.

conscious perception decoding electrophysiology global neuronal workspace theory integrated information theory neuronal populations non-human primate prefrontal cortex

Journal

Neuroscience of consciousness
ISSN: 2057-2107
Titre abrégé: Neurosci Conscious
Pays: England
ID NLM: 101679109

Informations de publication

Date de publication:
2022
Historique:
received: 19 01 2021
revised: 09 12 2021
accepted: 27 01 2022
entrez: 28 2 2022
pubmed: 1 3 2022
medline: 1 3 2022
Statut: epublish

Résumé

The role of the primate prefrontal cortex (PFC) in conscious perception is debated. The global neuronal workspace theory of consciousness predicts that PFC neurons should contain a detailed code of the current conscious contents. Previous research showed that PFC is indeed activated in paradigms of conscious visual perception, including no-report paradigms where no voluntary behavioral report of the percept is given, thus avoiding a conflation of signals related to visual consciousness with signals related to the report. Still, it has been argued that prefrontal modulation could reflect post-perceptual processes that may be present even in the absence of report, such as thinking about the perceived stimulus, therefore reflecting a consequence rather than a direct correlate of conscious experience. Here, we investigate these issues by recording neuronal ensemble activity from the macaque ventrolateral PFC during briefly presented visual stimuli, either in isolated trials in which stimuli were clearly perceived or in sequences of rapid serial visual presentation (RSVP) in which perception and post-perceptual processing were challenged. We report that the identity of each stimulus could be decoded from PFC population activity even in the RSVP condition. The first visual signals could be detected at 60 ms after stimulus onset and information was maximal at 150 ms. However, in the RSVP condition, 200 ms after the onset of a stimulus, the decoding accuracy quickly dropped to chance level and the next stimulus started to be decodable. Interestingly, decoding in the ventrolateral PFC was stronger compared to posterior parietal cortex for both isolated and RSVP stimuli. These results indicate that neuronal populations in the macaque PFC reliably encode visual stimuli even under conditions that have been shown to challenge conscious perception and/or substantially reduce the probability of post-perceptual processing in humans. We discuss whether the observed activation reflects conscious access, phenomenal consciousness, or merely a preconscious bottom-up wave.

Identifiants

pubmed: 35223085
doi: 10.1093/nc/niac005
pii: niac005
pmc: PMC8868130
doi:

Types de publication

Journal Article

Langues

eng

Pagination

niac005

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press.

Références

Nat Neurosci. 2001 Mar;4(3):311-6
pubmed: 11224549
Cortex. 2018 Oct;107:166-179
pubmed: 28985895
Philos Trans R Soc Lond B Biol Sci. 1998 Nov 29;353(1377):1801-18
pubmed: 9854253
PLoS One. 2011;6(6):e20910
pubmed: 21677786
J Comp Neurol. 1975 Apr 1;160(3):339-61
pubmed: 1112928
Trends Cogn Sci. 2011 Dec;15(12):567-75
pubmed: 22078929
PLoS Biol. 2009 Aug;7(8):e1000170
pubmed: 19668354
J Neurophysiol. 1992 Oct;68(4):1332-44
pubmed: 1432087
Neuron. 2021 Jan 6;109(1):164-176.e5
pubmed: 33080226
Front Syst Neurosci. 2008 Nov 24;2:4
pubmed: 19104670
Brain. 2009 Sep;132(Pt 9):2531-40
pubmed: 19433438
J Neurosci. 2015 Sep 30;35(39):13402-18
pubmed: 26424887
Curr Biol. 2013 Nov 4;23(21):2121-9
pubmed: 24139742
J Neurophysiol. 2004 Mar;91(3):1381-402
pubmed: 14573558
Nat Neurosci. 1999 Mar;2(3):283-8
pubmed: 10195223
Neuron. 2011 Apr 28;70(2):200-27
pubmed: 21521609
Nat Neurosci. 2001 Jul;4(7):752-8
pubmed: 11426233
Science. 2018 May 4;360(6388):537-542
pubmed: 29567809
J Neurosci. 2010 Mar 17;30(11):4143-50
pubmed: 20237284
Vis Neurosci. 1995 Mar-Apr;12(2):371-84
pubmed: 7786857
Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8378-83
pubmed: 12034865
Cereb Cortex. 2017 Jul 1;27(7):3683-3697
pubmed: 27371761
PLoS One. 2016 Feb 10;11(2):e0148504
pubmed: 26863625
Nat Commun. 2018 May 25;9(1):2057
pubmed: 29802308
Nat Rev Neurosci. 2016 Jul;17(7):450-61
pubmed: 27225071
Epilepsy Behav. 2020 Mar;104(Pt A):106644
pubmed: 31951969
PLoS Comput Biol. 2017 Nov 27;13(11):e1005806
pubmed: 29176808
Neuron. 2016 Dec 7;92(5):1122-1134
pubmed: 27930903
J Neurosci. 2021 Mar 10;41(10):2076-2087
pubmed: 33692142
Nat Neurosci. 2005 Oct;8(10):1391-400
pubmed: 16158062
Nat Hum Behav. 2020 Oct;4(10):1039-1052
pubmed: 32632334
PLoS Biol. 2009 Mar 17;7(3):e61
pubmed: 19296722
Philos Trans R Soc Lond B Biol Sci. 2002 Aug 29;357(1424):987-1001
pubmed: 12217170
J Neurosci. 2011 Jan 5;31(1):64-9
pubmed: 21209190
J Neurosci. 2017 Oct 4;37(40):9603-9613
pubmed: 28978697
J Vis. 2016 May 1;16(7):3
pubmed: 27139584
Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3599-604
pubmed: 18299568
Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8520-5
pubmed: 12829797
Cogn Neuropsychol. 2000 Feb 1;17(1):281-91
pubmed: 20945184
Trends Cogn Sci. 2011 Aug;15(8):365-73
pubmed: 21737339
J Neural Eng. 2019 Jun;16(3):036011
pubmed: 30822756
J Neurophysiol. 1998 Jun;79(6):3272-8
pubmed: 9636126
Percept Psychophys. 1987 Aug;42(2):105-13
pubmed: 3627930
Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1669-73
pubmed: 9990082
J Neurosci. 2014 Jan 29;34(5):1738-47
pubmed: 24478356
Neuron. 2012 Jun 7;74(5):924-35
pubmed: 22681695
J Neurophysiol. 2020 Jun 1;123(6):2311-2325
pubmed: 32401171
Nat Neurosci. 2016 Apr;19(4):613-22
pubmed: 26900926
Science. 2005 Nov 4;310(5749):863-6
pubmed: 16272124
Front Syst Neurosci. 2019 Mar 12;13:9
pubmed: 30914928
J Exp Psychol Gen. 1986 Sep;115(3):281-94
pubmed: 2944988
Neuron. 2009 Aug 27;63(4):508-22
pubmed: 19709632
Science. 2001 Jan 12;291(5502):312-6
pubmed: 11209083
Nat Commun. 2018 Jul 20;9(1):2852
pubmed: 30030440
Commun Biol. 2018 Dec 5;1:215
pubmed: 30534607
J Comp Neurol. 1985 Dec 22;242(4):535-60
pubmed: 2418080
Cogn Neurosci. 2010 Sep;1(3):165-75
pubmed: 24168333
Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18763-8
pubmed: 17124173
J Neurosci Methods. 2007 Aug 15;164(1):177-90
pubmed: 17517438
Proc Natl Acad Sci U S A. 2015 Apr 21;112(16):E2083-92
pubmed: 25847997
Curr Opin Neurobiol. 1999 Apr;9(2):189-94
pubmed: 10322191
J Neurophysiol. 2005 Sep;94(3):2086-92
pubmed: 15944228
Psychol Res. 2007 Mar;71(2):126-39
pubmed: 16341546
Neuron. 2019 Jul 17;103(2):292-308.e4
pubmed: 31171448
Trends Cogn Sci. 2020 Mar;24(3):167-168
pubmed: 31987718
Nat Commun. 2021 May 18;12(1):2930
pubmed: 34006884
Front Neurol. 2016 Jul 18;7:114
pubmed: 27486431
PLoS One. 2014 Jan 27;9(1):e85791
pubmed: 24475052
Curr Biol. 2013 Jan 21;23(2):150-5
pubmed: 23246406
Spat Vis. 1997;10(4):433-6
pubmed: 9176952
Cereb Cortex. 1999 Jul-Aug;9(5):459-75
pubmed: 10450891
J Neurosci. 2014 Mar 19;34(12):4382-95
pubmed: 24647958
Epilepsy Behav. 2000 Oct;1(5):356-61
pubmed: 12609167
Trends Cogn Sci. 2019 Sep;23(9):754-768
pubmed: 31375408
Vision Res. 1984;24(5):471-8
pubmed: 6740966
J Exp Psychol Hum Percept Perform. 1992 Aug;18(3):849-60
pubmed: 1500880
Trends Cogn Sci. 2014 Apr;18(4):203-10
pubmed: 24593982
Nat Rev Neurosci. 2016 May;17(5):307-21
pubmed: 27094080
Trends Cogn Sci. 2020 May;24(5):343-344
pubmed: 32298618
Curr Biol. 2017 Oct 9;27(19):2991-2998.e2
pubmed: 28943091
Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):449-54
pubmed: 16407167
Neuron. 2020 Mar 4;105(5):776-798
pubmed: 32135090
Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5587-91
pubmed: 7777553
Nat Commun. 2017 Dec 5;8(1):1955
pubmed: 29208892

Auteurs

Joachim Bellet (J)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Marion Gay (M)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Abhilash Dwarakanath (A)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Bechir Jarraya (B)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Timo van Kerkoerle (T)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Stanislas Dehaene (S)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Theofanis I Panagiotaropoulos (TI)

Cognitive Neuroimaging Unit, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, INSERM, Université Paris-Saclay, NeuroSpin, Gif-Sur-Yvette 91191, France.

Classifications MeSH