Data-driven analysis of simultaneous EEG/fMRI reveals neurophysiological phenotypes of impulse control
Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto‐striatal network is involved in these processes. Between‐subject differences in the intra‐individual variability have been suggested to constitute a key to pathological processes underlyi...
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| Published in | Human brain mapping Vol. 37; no. 9; pp. 3114 - 3136 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.09.2016
John Wiley & Sons, Inc John Wiley and Sons Inc |
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| Online Access | Get full text |
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| Abstract | Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto‐striatal network is involved in these processes. Between‐subject differences in the intra‐individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single‐trial EEG/fMRI analysis allows to increase sensitivity for inter‐individual differences by incorporating intra‐individual variability. Thirty‐eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo‐related ICs (Nogo‐IC‐positive) while 17 subjects (Nogo‐IC‐negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo‐IC‐negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra‐individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo‐IC‐negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data‐driven approach for IC classification and the resulting presence or absence of early Nogo‐specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter‐individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter‐individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo‐IC‐positive phenotype possibly providing protection against impulsivity‐related dysfunction. Hum Brain Mapp 37:3114–3136, 2016. © 2016 Wiley Periodicals, Inc. |
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| AbstractList | Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto-striatal network is involved in these processes. Between-subject differences in the intra-individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single-trial EEG/fMRI analysis allows to increase sensitivity for inter-individual differences by incorporating intra-individual variability. Thirty-eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo-related ICs (Nogo-IC-positive) while 17 subjects (Nogo-IC-negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo-IC-negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra-individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo-IC-negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data-driven approach for IC classification and the resulting presence or absence of early Nogo-specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter-individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter-individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo-IC-positive phenotype possibly providing protection against impulsivity-related dysfunction. Hum Brain Mapp 37:3114-3136, 2016. copyright 2016 Wiley Periodicals, Inc. Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto‐striatal network is involved in these processes. Between‐subject differences in the intra‐individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single‐trial EEG/fMRI analysis allows to increase sensitivity for inter‐individual differences by incorporating intra‐individual variability. Thirty‐eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo‐related ICs (Nogo‐IC‐positive) while 17 subjects (Nogo‐IC‐negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo‐IC‐negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra‐individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo‐IC‐negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data‐driven approach for IC classification and the resulting presence or absence of early Nogo‐specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter‐individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter‐individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo‐IC‐positive phenotype possibly providing protection against impulsivity‐related dysfunction. Hum Brain Mapp 37:3114–3136, 2016 . © 2016 Wiley Periodicals, Inc . Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto‐striatal network is involved in these processes. Between‐subject differences in the intra‐individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single‐trial EEG/fMRI analysis allows to increase sensitivity for inter‐individual differences by incorporating intra‐individual variability. Thirty‐eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo‐related ICs (Nogo‐IC‐positive) while 17 subjects (Nogo‐IC‐negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo‐IC‐negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra‐individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo‐IC‐negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data‐driven approach for IC classification and the resulting presence or absence of early Nogo‐specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter‐individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter‐individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo‐IC‐positive phenotype possibly providing protection against impulsivity‐related dysfunction. Hum Brain Mapp 37:3114–3136, 2016. © 2016 Wiley Periodicals, Inc. Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto-striatal network is involved in these processes. Between-subject differences in the intra-individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single-trial EEG/fMRI analysis allows to increase sensitivity for inter-individual differences by incorporating intra-individual variability. Thirty-eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo-related ICs (Nogo-IC-positive) while 17 subjects (Nogo-IC-negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo-IC-negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra-individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo-IC-negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data-driven approach for IC classification and the resulting presence or absence of early Nogo-specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter-individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter-individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo-IC-positive phenotype possibly providing protection against impulsivity-related dysfunction. Hum Brain Mapp 37:3114-3136, 2016. © 2016 Wiley Periodicals, Inc.Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto-striatal network is involved in these processes. Between-subject differences in the intra-individual variability have been suggested to constitute a key to pathological processes underlying impulse control disorders. Single-trial EEG/fMRI analysis allows to increase sensitivity for inter-individual differences by incorporating intra-individual variability. Thirty-eight healthy subjects performed a visual Go/Nogo task during simultaneous EEG/fMRI. Of 38 healthy subjects, 21 subjects reliably showed Nogo-related ICs (Nogo-IC-positive) while 17 subjects (Nogo-IC-negative) did not. Comparing both groups revealed differences on various levels: On trait level, Nogo-IC-negative subjects scored higher on questionnaires regarding attention deficit/hyperactivity disorder; on a behavioral level, they displayed slower response times (RT) and higher intra-individual RT variability while both groups did not differ in their inhibitory performance. On the neurophysiological level, Nogo-IC-negative subjects showed a hyperactivation of left inferior frontal cortex/insula and left putamen as well as significantly reduced P3 amplitudes. Thus, a data-driven approach for IC classification and the resulting presence or absence of early Nogo-specific ICs as criterion for group selection revealed group differences at behavioral and neurophysiological levels. This may indicate electrophysiological phenotypes characterized by inter-individual variations of neural and behavioral correlates of impulse control. We demonstrated that the inter-individual difference in an electrophysiological correlate of response inhibition is correlated with distinct, potentially compensatory neural activity. This may suggest the existence of electrophysiologically dissociable phenotypes of behavioral and neural motor response inhibition with the Nogo-IC-positive phenotype possibly providing protection against impulsivity-related dysfunction. Hum Brain Mapp 37:3114-3136, 2016. © 2016 Wiley Periodicals, Inc. |
| Author | Schmüser, Lena Lieb, Klaus Tüscher, Oliver Feige, Bernd Sebastian, Alexandra Mobascher, Arian |
| AuthorAffiliation | 3 Department of Psychiatry and Psychotherapy Albert Ludwigs University of Freiburg Medical Center Freiburg Germany 4 Department of Neurology Albert Ludwigs University of Freiburg Medical Center Freiburg Germany 2 Department of Psychiatry and Psychotherapy St. Elisabeth Krankenhaus Lahnstein Lahnstein Germany 1 Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz Mainz Germany |
| AuthorAffiliation_xml | – name: 3 Department of Psychiatry and Psychotherapy Albert Ludwigs University of Freiburg Medical Center Freiburg Germany – name: 1 Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz Mainz Germany – name: 2 Department of Psychiatry and Psychotherapy St. Elisabeth Krankenhaus Lahnstein Lahnstein Germany – name: 4 Department of Neurology Albert Ludwigs University of Freiburg Medical Center Freiburg Germany |
| Author_xml | – sequence: 1 givenname: Lena surname: Schmüser fullname: Schmüser, Lena email: lena.schmueser@unimedizin-mainz.de organization: Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz, Mainz, Germany – sequence: 2 givenname: Alexandra surname: Sebastian fullname: Sebastian, Alexandra organization: Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz, Mainz, Germany – sequence: 3 givenname: Arian surname: Mobascher fullname: Mobascher, Arian organization: Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz, Mainz, Germany – sequence: 4 givenname: Klaus surname: Lieb fullname: Lieb, Klaus organization: Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz, Mainz, Germany – sequence: 5 givenname: Bernd surname: Feige fullname: Feige, Bernd organization: Department of Psychiatry and Psychotherapy, Albert Ludwigs University of Freiburg Medical Center, Freiburg, Germany – sequence: 6 givenname: Oliver surname: Tüscher fullname: Tüscher, Oliver organization: Emotion Regulation and Impulse Control Group, Focus Program Translational Neuroscience, Department of Psychiatry and Psychotherapy, Johannes Gutenberg University of Mainz, Mainz, Germany |
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| Keywords | inter-individual differences electrophysiological phenotypes simultaneous EEG/fMRI independent component analysis (ICA) response inhibition Go/Nogo |
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| Snippet | Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto‐striatal network is involved in these... Response inhibition is the ability to suppress inadequate but prepotent or ongoing response tendencies. A fronto-striatal network is involved in these... |
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| SubjectTerms | Adult Brain - physiology Disruptive, Impulse Control, and Conduct Disorders - physiopathology Electroencephalography electrophysiological phenotypes Female Go/Nogo Humans Image Processing, Computer-Assisted Impulsive Behavior - physiology independent component analysis (ICA) Inhibition (Psychology) inter-individual differences Magnetic Resonance Imaging Male response inhibition Signal Processing, Computer-Assisted simultaneous EEG/fMRI |
| Title | Data-driven analysis of simultaneous EEG/fMRI reveals neurophysiological phenotypes of impulse control |
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