Synchronization patterns reveal neuronal coding of working memory content.

MVPA auditory functional connectivity machine learning magnetoencephalography phase synchronization working memory

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
24 08 2021
Historique:
received: 17 09 2020
revised: 26 04 2021
accepted: 28 07 2021
entrez: 25 8 2021
pubmed: 26 8 2021
medline: 12 2 2022
Statut: ppublish

Résumé

Neuronal oscillations are suggested to play an important role in auditory working memory (WM), but their contribution to content-specific representations has remained unclear. Here, we measure magnetoencephalography during a retro-cueing task with parametric ripple-sound stimuli, which are spectrotemporally similar to speech but resist non-auditory memory strategies. Using machine learning analyses, with rigorous between-subject cross-validation and non-parametric permutation testing, we show that memorized sound content is strongly represented in phase-synchronization patterns between subregions of auditory and frontoparietal cortices. These phase-synchronization patterns predict the memorized sound content steadily across the studied maintenance period. In addition to connectivity-based representations, there are indices of more local, "activity silent" representations in auditory cortices, where the decoding accuracy of WM content significantly increases after task-irrelevant "impulse stimuli." Our results demonstrate that synchronization patterns across auditory sensory and association areas orchestrate neuronal coding of auditory WM content. This connectivity-based coding scheme could also extend beyond the auditory domain.

Identifiants

pubmed: 34433024
pii: S2211-1247(21)01000-7
doi: 10.1016/j.celrep.2021.109566
pmc: PMC8428113
mid: NIHMS1735642
pii:
doi:

Types de publication

Clinical Trial Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

109566

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC016915
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS104585
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC017991
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC016765
Pays : United States
Organisme : NIBIB NIH HHS
ID : P41 EB015896
Pays : United States

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

J Neurosci. 2018 Aug 8;38(32):7020-7028
pubmed: 30089641
Clin Neurophysiol. 2004 Oct;115(10):2292-307
pubmed: 15351371
Sci Rep. 2019 May 28;9(1):7942
pubmed: 31138854
Science. 2009 May 29;324(5931):1207-10
pubmed: 19478185
Trends Neurosci. 2007 Jul;30(7):309-16
pubmed: 17555828
Annu Rev Neurosci. 2014;37:435-56
pubmed: 25002277
Trends Cogn Sci. 2005 Oct;9(10):474-80
pubmed: 16150631
Proc Natl Acad Sci U S A. 2011 Aug 2;108(31):12961-6
pubmed: 21768383
Neuropsychologia. 1997 Jun;35(6):795-812
pubmed: 9204486
Front Neurosci. 2018 Mar 27;12:174
pubmed: 29636657
PLoS Biol. 2007 Mar;5(3):e56
pubmed: 17311472
Neuroimage. 2014 Feb 1;86:446-60
pubmed: 24161808
Neuroimage. 2018 Jul 1;174:57-68
pubmed: 29462724
Nat Neurosci. 2016 Jan;19(1):150-7
pubmed: 26595654
Exp Brain Res. 1989;74(1):139-48
pubmed: 2924831
Cereb Cortex. 2007 Oct;17(10):2364-74
pubmed: 17190968
Neuroimage. 2003 Oct;20(2):816-27
pubmed: 14568454
Front Neurosci. 2014 Aug 14;8:250
pubmed: 25177266
Trends Cogn Sci. 2014 Jan;18(1):16-25
pubmed: 24268290
Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14611-6
pubmed: 19667199
Hum Brain Mapp. 2019 Apr 15;40(6):1856-1866
pubmed: 30537025
Neuroimage. 2004 Jan;21(1):340-51
pubmed: 14741672
J Neurosci. 2016 Apr 20;36(16):4492-505
pubmed: 27098693
J Neurophysiol. 2014 Feb;111(3):455-69
pubmed: 24198324
Trends Cogn Sci. 2017 Feb;21(2):111-124
pubmed: 28063661
Hum Brain Mapp. 2018 Oct;39(10):4094-4104
pubmed: 29947148
J Neurosci. 2012 Sep 19;32(38):12983-9
pubmed: 22993415
J Cogn Neurosci. 2013 May;25(5):754-61
pubmed: 23469889
Hum Brain Mapp. 2006 Jan;27(1):1-13
pubmed: 16082624
Cogn Psychol. 1997 Jun;33(1):5-42
pubmed: 9212720
Proc Natl Acad Sci U S A. 2010 Apr 20;107(16):7580-5
pubmed: 20368447
Curr Opin Neurobiol. 2014 Apr;25:20-4
pubmed: 24709596
Brain Topogr. 2004 Summer;16(4):269-75
pubmed: 15379226
Science. 2012 Nov 23;338(6110):1097-100
pubmed: 23118014
Neuroimage. 2013 Dec;83:1098-108
pubmed: 23921102
Science. 2008 Mar 14;319(5869):1543-6
pubmed: 18339943
Neuroimage. 1999 Feb;9(2):179-94
pubmed: 9931268
Elife. 2016 Jul 20;5:
pubmed: 27438411
Nat Neurosci. 2015 Apr;18(4):484-9
pubmed: 25706474
Annu Rev Physiol. 2002;64:355-405
pubmed: 11826273
Neuron. 2018 Oct 24;100(2):463-475
pubmed: 30359609
Brain Res. 2016 Jun 1;1640(Pt B):264-77
pubmed: 26541581
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Science. 1971 Aug 13;173(3997):652-4
pubmed: 4998337
Nat Commun. 2019 Feb 25;10(1):936
pubmed: 30804436
Front Syst Neurosci. 2015 Sep 03;9:123
pubmed: 26388748
Curr Biol. 2014 Dec 1;24(23):2767-75
pubmed: 25456448
Neuron. 2012 Nov 21;76(4):838-846
pubmed: 23177967
Neuron. 2016 Aug 3;91(3):694-707
pubmed: 27497224
Vision Res. 2016 Nov;128:53-67
pubmed: 27668990
J Neurosci Methods. 2007 Aug 15;164(1):177-90
pubmed: 17517438
Neuroimage. 2009 Jul 15;46(4):1127-36
pubmed: 19289171
Neuron. 2005 Nov 23;48(4):687-97
pubmed: 16301183
Behav Brain Res. 2009 Dec 14;205(1):299-302
pubmed: 19712703
J Neurosci. 2010 Feb 17;30(7):2694-9
pubmed: 20164353
Science. 1999 Mar 12;283(5408):1657-61
pubmed: 10073923
Neuroscience. 2006 Apr 28;139(1):23-38
pubmed: 16324795
Trends Cogn Sci. 2014 Feb;18(2):82-9
pubmed: 24439529
Neuropsychologia. 2021 Jan 8;150:107691
pubmed: 33227284
Science. 2016 Dec 2;354(6316):1136-1139
pubmed: 27934762
Nat Neurosci. 2010 Aug;13(8):1011-9
pubmed: 20622871
Front Neuroinform. 2016 Jul 22;10:27
pubmed: 27499741
J Neurosci. 2017 Jan 11;37(2):313-322
pubmed: 28077711
J Cogn Neurosci. 2010 Nov;22(11):2530-40
pubmed: 19925206
Neuron. 2016 Apr 6;90(1):152-164
pubmed: 26996084
Elife. 2018 Jun 21;7:
pubmed: 29927384
Trends Cogn Sci. 2014 Apr;18(4):203-10
pubmed: 24593982
Neuroimage. 2018 Dec;183:254-262
pubmed: 30107259
Ann N Y Acad Sci. 2009 Jul;1169:273-7
pubmed: 19673792
Dev Cogn Neurosci. 2018 Nov;34:114-123
pubmed: 30336447
PLoS One. 2016 Jan 08;11(1):e0146443
pubmed: 26745498
Cereb Cortex. 2003 Dec;13(12):1369-74
pubmed: 14615302
Nat Neurosci. 2017 Jun;20(6):864-871
pubmed: 28414333
Cereb Cortex. 2018 Jun 1;28(6):2146-2161
pubmed: 28505235
Trends Cogn Sci. 2015 Jul;19(7):394-405
pubmed: 26051384
J Neurosci. 2002 Jul 1;22(13):5630-8
pubmed: 12097514
Neuroimage. 1999 Feb;9(2):195-207
pubmed: 9931269
PLoS One. 2015 Feb 13;10(2):e0116118
pubmed: 25680187
Cereb Cortex. 2008 Oct;18(10):2286-95
pubmed: 18252742
Nat Commun. 2020 Apr 14;11(1):1832
pubmed: 32286288
Trends Cogn Sci. 2017 Oct;21(10):794-815
pubmed: 28774684
J Neurosci. 2020 Jan 15;40(3):671-681
pubmed: 31754009
J Neurosci. 2012 Sep 5;32(36):12411-20
pubmed: 22956832

Auteurs

Fahimeh Mamashli (F)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Sheraz Khan (S)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Matti Hämäläinen (M)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Mainak Jas (M)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Tommi Raij (T)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA; Departments of Physical Medicine and Rehabilitation and Neurobiology, Northwestern University, 710 North Lake Shore Drive, Chicago, IL 60611, USA.

Steven M Stufflebeam (SM)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Aapo Nummenmaa (A)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA.

Jyrki Ahveninen (J)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Bldg. 149 13(th) Street, Charlestown, MA 02129, USA; Department of Radiology, Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA. Electronic address: jahveninen@mgh.harvard.edu.

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