Pupillary Dynamics Link Spontaneous and Task-Evoked Activations Recorded Directly from Human Insula.

Tytuł:: Pupillary Dynamics Link Spontaneous and Task-Evoked Activations Recorded Directly from Human Insula.
Autorzy:: Kucyi A; Department of Psychology, Northeastern University, Boston, Massachusetts 02115.
Parvizi J; Department of Neurology & Neurological Sciences, Stanford University, Stanford, California 94304 .
Źródło:: The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2020 Aug 05; Vol. 40 (32), pp. 6207-6218. Date of Electronic Publication: 2020 Jul 06.
Typ publikacji:: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: Washington, DC : Society for Neuroscience
Original Publication: [Baltimore, Md.] : The Society, c1981-
MeSH Terms:: Attention*
Evoked Potentials*
Cerebral Cortex/*physiology
Pupil/*physiology
Adult ; Female ; Humans ; Male ; Reaction Time
References:: Neuroimage. 2016 Oct 1;139:189-201. (PMID: 27291493)
Neuroimage. 2010 May 1;50(4):1690-701. (PMID: 20079856)
J Neurosci. 2014 Jan 8;34(2):408-17. (PMID: 24403141)
Trends Cogn Sci. 2020 Jun;24(6):466-480. (PMID: 32331857)
Comput Intell Neurosci. 2011;2011:156869. (PMID: 21253357)
J Neurophysiol. 2016 Feb 1;115(2):662-73. (PMID: 26538607)
Nat Rev Neurosci. 2015 Jan;16(1):55-61. (PMID: 25406711)
J Neurosci. 2013 Jun 19;33(25):10503-11. (PMID: 23785162)
Hum Brain Mapp. 2019 Jun 15;40(9):2611-2622. (PMID: 30815964)
Neuron. 2006 Jun 1;50(5):799-812. (PMID: 16731517)
Neuroimage. 2015 Feb 1;106:414-27. (PMID: 25463449)
J Neurosci. 2007 Feb 28;27(9):2349-56. (PMID: 17329432)
Neuron. 2015 Feb 4;85(3):628-40. (PMID: 25654259)
Nat Neurosci. 2018 Apr;21(4):474-483. (PMID: 29507407)
J Neurosci. 2018 Apr 25;38(17):4230-4242. (PMID: 29626167)
Hum Brain Mapp. 1999;8(4):272-84. (PMID: 10619420)
Proc Natl Acad Sci U S A. 2018 May 1;115(18):4785-4790. (PMID: 29666262)
Insight J. 2006;2006:209. (PMID: 25364771)
Neuroimage. 2013 Jul 1;74:188-94. (PMID: 23485741)
Neuron. 2015 Oct 7;88(1):194-206. (PMID: 26447581)
Cereb Cortex. 2013 Nov;23(11):2712-23. (PMID: 22941724)
Neurology. 1992 Sep;42(9):1727-32. (PMID: 1513461)
Cognition. 2017 Nov;168:16-26. (PMID: 28645038)
Nat Commun. 2013;4:2528. (PMID: 24129341)
Proc Natl Acad Sci U S A. 2016 Apr 26;113(17):E2430-9. (PMID: 27071080)
J Comp Neurol. 1982 Nov 20;212(1):38-52. (PMID: 7174907)
Nat Commun. 2020 Jan 16;11(1):325. (PMID: 31949140)
J Neurosci. 2017 Jan 11;37(2):281-290. (PMID: 28077708)
Nat Commun. 2016 Nov 08;7:13289. (PMID: 27824036)
Neuron. 2014 Oct 22;84(2):355-62. (PMID: 25374359)
Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):13040-5. (PMID: 19620724)
Mayo Clin Proc. 1993 Oct;68(10):988-1001. (PMID: 8412366)
Neuron. 2016 Jan 6;89(1):221-34. (PMID: 26711118)
J Neurosci. 2014 Dec 3;34(49):16286-95. (PMID: 25471568)
J Neurosci. 2014 Oct 29;34(44):14652-67. (PMID: 25355218)
Hum Brain Mapp. 2009 Sep;30(9):2731-45. (PMID: 19072897)
Cogn Affect Behav Neurosci. 2016 Aug;16(4):601-15. (PMID: 27038165)
Cell Rep. 2017 Sep 26;20(13):3099-3112. (PMID: 28954227)
Exp Physiol. 2014 Feb;99(2):326-31. (PMID: 24121283)
Neuroimage. 2004 Jun;22(2):492-502. (PMID: 15193578)
J Neurosci. 2007 Feb 28;27(9):2424-32. (PMID: 17329441)
PLoS One. 2011 Mar 25;6(3):e18298. (PMID: 21464969)
Neuroimage. 2013 Mar;68:93-104. (PMID: 23246859)
J Comp Neurol. 1987 Aug 8;262(2):271-89. (PMID: 3624555)
Nat Rev Neurosci. 2009 Jan;10(1):59-70. (PMID: 19096369)
J Neurosci Methods. 2017 Apr 1;281:40-48. (PMID: 28192130)
Eur J Neurosci. 2014 Sep;40(5):2822-32. (PMID: 24911340)
Science. 2011 Nov 25;334(6059):1151-3. (PMID: 22116887)
Neuron. 2016 Oct 19;92(2):544-554. (PMID: 27693256)
Nat Rev Neurosci. 2015 Jul;16(7):419-29. (PMID: 26016744)
Cereb Cortex. 2017 Feb 1;27(2):1545-1557. (PMID: 26796212)
Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):3023-8. (PMID: 21282630)
J Neurosci Methods. 2007 Aug 15;164(1):177-90. (PMID: 17517438)
J Cogn. 2018 Feb 21;1(1):16. (PMID: 31517190)
Neuron. 2015 Apr 22;86(2):578-90. (PMID: 25863718)
Neuron. 2015 Sep 23;87(6):1143-1161. (PMID: 26402600)
Eur J Neurosci. 2017 Jan;45(2):260-266. (PMID: 27712047)
Hum Brain Mapp. 2014 Aug;35(8):4140-54. (PMID: 24510607)
Neuron. 2020 Mar 18;105(6):1094-1111.e10. (PMID: 31955944)
Science. 2016 Apr 8;352(6282):216-20. (PMID: 27124457)
Brain Struct Funct. 2010 Jun;214(5-6):655-67. (PMID: 20512370)
Behav Res Methods. 2010 Aug;42(3):671-84. (PMID: 20805589)
Spat Vis. 1997;10(4):433-6. (PMID: 9176952)
Annu Rev Neurosci. 2005;28:403-50. (PMID: 16022602)
Nat Neurosci. 2008 Sep;11(9):1100-8. (PMID: 19160509)
Nat Rev Neurosci. 2007 Sep;8(9):700-11. (PMID: 17704812)
Ann Neurol. 2016 May;79(5):709-716. (PMID: 30240034)
Neuroimage. 2005 Oct 1;27(4):885-95. (PMID: 15996878)
Curr Opin Neurobiol. 2015 Aug;33:134-40. (PMID: 25863645)
Science. 2019 Apr 19;364(6437):255. (PMID: 31000656)
J Neurophysiol. 2002 Jan;87(1):615-20. (PMID: 11784775)
Neuroimage. 2018 May 1;171:148-164. (PMID: 29307606)
Neuroimage. 2019 Aug 15;197:383-390. (PMID: 31055043)
Nat Commun. 2015 Jul 16;6:7751. (PMID: 26178017)
Trends Cogn Sci. 2014 Apr;18(4):177-85. (PMID: 24440116)
Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13899-13904. (PMID: 27856733)
Netw Neurosci. 2018 Oct 01;2(4):397-417. (PMID: 30465033)
Nat Commun. 2018 Jun 25;9(1):2455. (PMID: 29941957)
J Neurophysiol. 2011 Sep;106(3):1125-65. (PMID: 21653723)
Behav Res Methods. 2010 Feb;42(1):212-25. (PMID: 20160301)
J Neurosci. 2012 Aug 15;32(33):11176-86. (PMID: 22895703)
Age Ageing. 1996 Nov;25(6):432-8. (PMID: 9003878)
Proc Natl Acad Sci U S A. 2013 Mar 12;110(11):4392-7. (PMID: 23440216)
Neuron. 2019 Aug 21;103(4):702-718.e5. (PMID: 31227310)
Grant Information:: R01 MH109954 United States MH NIMH NIH HHS; R01 NS078396 United States NS NINDS NIH HHS; Canada CIHR
Contributed Indexing:: Keywords: arousal; attention; intracranial EEG; pupillometry; resting state; sympathetic
Entry Date(s):: Date Created: 20200708 Date Completed: 20210104 Latest Revision: 20210408
Update Code:: 20240105
PubMed Central ID:: PMC7406275
DOI:: 10.1523/JNEUROSCI.0435-20.2020
PMID:: 32631937
: Czasopismo naukowe

Spontaneous activations within neuronal populations can emerge similarly to "task-evoked" activations elicited during cognitive performance or sensory stimulation. We hypothesized that spontaneous activations within a given brain region have comparable functional and physiological properties to task-evoked activations. Using human intracranial EEG with concurrent pupillometry in 3 subjects (2 males, 1 female), we localized neuronal populations in the dorsal anterior insular cortex that showed task-evoked activations correlating positively with the magnitude of pupil dilation during a continuous performance task. The pupillary response peaks lagged behind insular activations by several hundreds of milliseconds. We then detected spontaneous activations, within the same neuronal populations of insular cortex, that emerged intermittently during a wakeful "resting state" and that had comparable electrophysiological properties (magnitude, duration, and spectral signature) to task-evoked activations. Critically, similar to task-evoked activations, spontaneous activations systematically preceded phasic pupil dilations with a strikingly similar temporal profile. Our findings suggest similar neurophysiological profiles between spontaneous and task-evoked activations in the human insula and support a clear link between these activations and autonomic functions measured by dynamics of pupillary dilation. SIGNIFICANCE STATEMENT Most of our knowledge about activations in the human brain is derived from studies of responses to external events and experimental conditions (i.e., "task-evoked" activations). We obtained direct neural recordings from electrodes implanted in human subjects and showed that activations emerge spontaneously and have strong similarities to task-evoked activations(e.g., magnitude, temporal profile) within the same populations of neurons. Within the dorsal anterior insula, a brain region implicated in salience processing and alertness, activations that are either spontaneous or task-evoked are coupled with brief dilations of the pupil. Our findings underscore how spontaneous brain activity, a major current focus of human neuroimaging studies aimed at developing biomarkers of disease, is relevant to ongoing physiological and possibly self-generated mental processes.
(Copyright © 2020 the authors.)

Comment in: J Neurosci. 2021 Apr 7;41(14):3051-3053. (PMID: 33827971)

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