FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity

Alessio Fracasso; Anna Gaglianese; Mariska J. Vansteensel; Erik J. Aarnoutse; Nick F. Ramsey; Serge O. Dumoulin; Natalia Petridou

doi:10.1007/s00429-021-02342-4

FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity

Alessio Fracasso^*, Anna Gaglianese, Mariska J. Vansteensel, Erik J. Aarnoutse, Nick F. Ramsey, Serge O. Dumoulin, Natalia Petridou

^*Corresponding author for this work

Cognitive Psychology

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Positive blood oxygenation level-dependent (BOLD) responses (PBR), as measured by functional Magnetic Resonance Imaging (fMRI), are the most utilized measurements to non-invasively map activity in the brain. Recent studies have consistently shown that BOLD responses are not exclusively positive. Negative BOLD responses (NBR) have been reported in response to specific sensory stimulations and tasks. However, the exact relationship between NBR and the underlying metabolic and neuronal demand is still under debate. In this study, we investigated the neurophysiological basis of negative BOLD using fMRI and intra-cranial electrophysiology (electrocorticography, ECoG) measurements from the same human participants. We show that, for those electrodes that responded to visual stimulation, PBR are correlated with high-frequency band (HFB) responses. Crucially, NBR were associated with an absence of HFB power responses and an unpredicted decrease in the alpha power responses.

Original language	English
Pages (from-to)	1371-1384
Number of pages	14
Journal	Brain Structure and Function
Volume	227
Issue number	4
Early online date	7 Aug 2021
DOIs	https://doi.org/10.1007/s00429-021-02342-4
Publication status	Published - May 2022

Bibliographical note

Funding Information:
This work was supported by the Netherlands Organization for Scientific Research (NWO), Vidi Grant number 13339 (N.P.), the European Research Council (ERC) Advanced ‘iConnect’ Project, number 320708 (N.F.R.), and the National Institute of Mental Health of the National Institutes of Health under award number R01MH111417 (N.P.) A.F. is supported by a grant from the Biotechnology and Biology research council (BBSRC, Grant number: BB/S006605/1) and the Bial Foundation, Bial Foundation Grants Program 2020/21, A-29315.

Publisher Copyright:
© 2021, The Author(s).

Funding

This work was supported by the Netherlands Organization for Scientific Research (NWO), Vidi Grant number 13339 (N.P.), the European Research Council (ERC) Advanced ‘iConnect’ Project, number 320708 (N.F.R.), and the National Institute of Mental Health of the National Institutes of Health under award number R01MH111417 (N.P.) A.F. is supported by a grant from the Biotechnology and Biology research council (BBSRC, Grant number: BB/S006605/1) and the Bial Foundation, Bial Foundation Grants Program 2020/21, A-29315.

Funders	Funder number
Biotechnology and Biology research council	BB/S006605/1
National Institutes of Health
National Institute of Mental Health	R01MH111417
European Research Council	320708
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	13339
Fundação Bial	2020/21, A-29315

Keywords

ECoG
Negative BOLD
Neuronal activity
Positive BOLD

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10.1007/s00429-021-02342-4

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@article{d813313deba940ee81b518b6c4d3161e,

title = "FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity",

abstract = "Positive blood oxygenation level-dependent (BOLD) responses (PBR), as measured by functional Magnetic Resonance Imaging (fMRI), are the most utilized measurements to non-invasively map activity in the brain. Recent studies have consistently shown that BOLD responses are not exclusively positive. Negative BOLD responses (NBR) have been reported in response to specific sensory stimulations and tasks. However, the exact relationship between NBR and the underlying metabolic and neuronal demand is still under debate. In this study, we investigated the neurophysiological basis of negative BOLD using fMRI and intra-cranial electrophysiology (electrocorticography, ECoG) measurements from the same human participants. We show that, for those electrodes that responded to visual stimulation, PBR are correlated with high-frequency band (HFB) responses. Crucially, NBR were associated with an absence of HFB power responses and an unpredicted decrease in the alpha power responses.",

keywords = "ECoG, Negative BOLD, Neuronal activity, Positive BOLD",

author = "Alessio Fracasso and Anna Gaglianese and Vansteensel, {Mariska J.} and Aarnoutse, {Erik J.} and Ramsey, {Nick F.} and Dumoulin, {Serge O.} and Natalia Petridou",

note = "Funding Information: This work was supported by the Netherlands Organization for Scientific Research (NWO), Vidi Grant number 13339 (N.P.), the European Research Council (ERC) Advanced {\textquoteleft}iConnect{\textquoteright} Project, number 320708 (N.F.R.), and the National Institute of Mental Health of the National Institutes of Health under award number R01MH111417 (N.P.) A.F. is supported by a grant from the Biotechnology and Biology research council (BBSRC, Grant number: BB/S006605/1) and the Bial Foundation, Bial Foundation Grants Program 2020/21, A-29315. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2022",

month = may,

doi = "10.1007/s00429-021-02342-4",

language = "English",

volume = "227",

pages = "1371--1384",

journal = "Brain Structure and Function",

issn = "1863-2653",

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FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity. / Fracasso, Alessio; Gaglianese, Anna; Vansteensel, Mariska J. et al.
In: Brain Structure and Function, Vol. 227, No. 4, 05.2022, p. 1371-1384.

Research output: Contribution to Journal › Article › Academic › peer-review

TY - JOUR

T1 - FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity

AU - Fracasso, Alessio

AU - Gaglianese, Anna

AU - Vansteensel, Mariska J.

AU - Aarnoutse, Erik J.

AU - Ramsey, Nick F.

AU - Dumoulin, Serge O.

AU - Petridou, Natalia

N1 - Funding Information: This work was supported by the Netherlands Organization for Scientific Research (NWO), Vidi Grant number 13339 (N.P.), the European Research Council (ERC) Advanced ‘iConnect’ Project, number 320708 (N.F.R.), and the National Institute of Mental Health of the National Institutes of Health under award number R01MH111417 (N.P.) A.F. is supported by a grant from the Biotechnology and Biology research council (BBSRC, Grant number: BB/S006605/1) and the Bial Foundation, Bial Foundation Grants Program 2020/21, A-29315. Publisher Copyright: © 2021, The Author(s).

PY - 2022/5

Y1 - 2022/5

N2 - Positive blood oxygenation level-dependent (BOLD) responses (PBR), as measured by functional Magnetic Resonance Imaging (fMRI), are the most utilized measurements to non-invasively map activity in the brain. Recent studies have consistently shown that BOLD responses are not exclusively positive. Negative BOLD responses (NBR) have been reported in response to specific sensory stimulations and tasks. However, the exact relationship between NBR and the underlying metabolic and neuronal demand is still under debate. In this study, we investigated the neurophysiological basis of negative BOLD using fMRI and intra-cranial electrophysiology (electrocorticography, ECoG) measurements from the same human participants. We show that, for those electrodes that responded to visual stimulation, PBR are correlated with high-frequency band (HFB) responses. Crucially, NBR were associated with an absence of HFB power responses and an unpredicted decrease in the alpha power responses.

AB - Positive blood oxygenation level-dependent (BOLD) responses (PBR), as measured by functional Magnetic Resonance Imaging (fMRI), are the most utilized measurements to non-invasively map activity in the brain. Recent studies have consistently shown that BOLD responses are not exclusively positive. Negative BOLD responses (NBR) have been reported in response to specific sensory stimulations and tasks. However, the exact relationship between NBR and the underlying metabolic and neuronal demand is still under debate. In this study, we investigated the neurophysiological basis of negative BOLD using fMRI and intra-cranial electrophysiology (electrocorticography, ECoG) measurements from the same human participants. We show that, for those electrodes that responded to visual stimulation, PBR are correlated with high-frequency band (HFB) responses. Crucially, NBR were associated with an absence of HFB power responses and an unpredicted decrease in the alpha power responses.

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ER -

FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity

Abstract

Bibliographical note

Funding

Keywords

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