Reduced premovement positivity during the stimulus-response interval precedes errors: Using single-trial and regression ERPs to understand performance deficits in ADHD

Scott J. Burwell; Scott Makeig; William G. Iacono; Stephen M. Malone

doi:10.1111/psyp.13392

Reduced premovement positivity during the stimulus-response interval precedes errors: Using single-trial and regression ERPs to understand performance deficits in ADHD

Scott J. Burwell, Scott Makeig, William G. Iacono, Stephen M. Malone

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Brain mechanisms linked to incorrect response selections made under time pressure during cognitive task performance are poorly understood, particularly in adolescents with attention-deficit hyperactivity disorder (ADHD). Using subject-specific multimodal imaging (electroencephalogram, magnetic resonance imaging, behavior) during flanker task performance by a sample of 94 human adolescents (mean age = 15.5 years, 50% female) with varying degrees of ADHD symptomatology, we examined the degree to which amplitude features of source-resolved event-related potentials (ERPs) from brain-independent component processes within a critical (but often ignored) period in the action selection process, the stimulus-response interval, were associated with motor response errors (across trials) and error rates (across individuals). Response errors were typically preceded by two smaller peaks in both trial-level and trial-averaged ERP projections from posterior medial frontal cortex (pMFC): a frontocentral P3 peaking about 390 ms after stimulus onset, and a premovement positivity (PMP) peaking about 110 ms before the motor response. Separating overlapping stimulus-locked and response-locked ERP contributions using a “regression ERP” approach showed that trial errors and participant error rates were primarily associated with smaller PMP, and not with frontocentral P3. Moreover, smaller PMP mediated the association between larger numbers of errors and ADHD symptoms, suggesting the possible value of using PMP as an intervention target to remediate performance deficits in ADHD.

Original language	English (US)
Article number	e13392
Journal	Psychophysiology
Volume	56
Issue number	9
DOIs	https://doi.org/10.1111/psyp.13392
State	Published - 2019

Bibliographical note

Funding Information:
This research was made possible by funding from grant number AA017314 from the National Institute of Alcohol Abuse and Alcoholism (NIAAA) as well as grant numbers DA036216 and DA05147 from the National Institute on Drug Abuse (NIDA). In addition, SJB is funded by a NIDA T32 postdoctoral fellowship (DA037183) and received funding from the Society for Psychophysiological Research that enabled mentorship from SM at the Swartz Center for Computational Neuroscience (SCCN) at UCSD. SJB would like to acknowledge Shelby Piepho for assistance with manual preprocessing of structural MRI images as part of an undergraduate research experience. Also, SJB would like to thank Dr. Zeynep Akalin Acar and Matthew Burns at the SCCN for providing feedback in computational head modeling and regression ERP procedures, respectively, as well as Dr. Philip Burton at UMN's Center for Magnetic Resonance Research for his expert guidance in the cross-subject dipole coregistration method. SM's participation was funded by a gift from The Swartz Foundation (Old Field, NY).

Publisher Copyright:
© 2019 Society for Psychophysiological Research

Keywords

ADHD
ERP
medial frontal cortex
performance monitoring
premovement positivity
stimulus-response interval

Publisher link

10.1111/psyp.13392

Find It

Find It at U of M Libraries

Cite this

@article{7e72bd6d8d6440efb27f1a263c53cedd,

title = "Reduced premovement positivity during the stimulus-response interval precedes errors: Using single-trial and regression ERPs to understand performance deficits in ADHD",

abstract = "Brain mechanisms linked to incorrect response selections made under time pressure during cognitive task performance are poorly understood, particularly in adolescents with attention-deficit hyperactivity disorder (ADHD). Using subject-specific multimodal imaging (electroencephalogram, magnetic resonance imaging, behavior) during flanker task performance by a sample of 94 human adolescents (mean age = 15.5 years, 50% female) with varying degrees of ADHD symptomatology, we examined the degree to which amplitude features of source-resolved event-related potentials (ERPs) from brain-independent component processes within a critical (but often ignored) period in the action selection process, the stimulus-response interval, were associated with motor response errors (across trials) and error rates (across individuals). Response errors were typically preceded by two smaller peaks in both trial-level and trial-averaged ERP projections from posterior medial frontal cortex (pMFC): a frontocentral P3 peaking about 390 ms after stimulus onset, and a premovement positivity (PMP) peaking about 110 ms before the motor response. Separating overlapping stimulus-locked and response-locked ERP contributions using a “regression ERP” approach showed that trial errors and participant error rates were primarily associated with smaller PMP, and not with frontocentral P3. Moreover, smaller PMP mediated the association between larger numbers of errors and ADHD symptoms, suggesting the possible value of using PMP as an intervention target to remediate performance deficits in ADHD.",

keywords = "ADHD, ERP, medial frontal cortex, performance monitoring, premovement positivity, stimulus-response interval",

author = "Burwell, {Scott J.} and Scott Makeig and Iacono, {William G.} and Malone, {Stephen M.}",

note = "Funding Information: This research was made possible by funding from grant number AA017314 from the National Institute of Alcohol Abuse and Alcoholism (NIAAA) as well as grant numbers DA036216 and DA05147 from the National Institute on Drug Abuse (NIDA). In addition, SJB is funded by a NIDA T32 postdoctoral fellowship (DA037183) and received funding from the Society for Psychophysiological Research that enabled mentorship from SM at the Swartz Center for Computational Neuroscience (SCCN) at UCSD. SJB would like to acknowledge Shelby Piepho for assistance with manual preprocessing of structural MRI images as part of an undergraduate research experience. Also, SJB would like to thank Dr. Zeynep Akalin Acar and Matthew Burns at the SCCN for providing feedback in computational head modeling and regression ERP procedures, respectively, as well as Dr. Philip Burton at UMN's Center for Magnetic Resonance Research for his expert guidance in the cross-subject dipole coregistration method. SM's participation was funded by a gift from The Swartz Foundation (Old Field, NY). Publisher Copyright: {\textcopyright} 2019 Society for Psychophysiological Research",

year = "2019",

doi = "10.1111/psyp.13392",

language = "English (US)",

volume = "56",

journal = "Psychophysiology",

issn = "0048-5772",

publisher = "Wiley-Blackwell",

number = "9",

}

TY - JOUR

T1 - Reduced premovement positivity during the stimulus-response interval precedes errors

T2 - Using single-trial and regression ERPs to understand performance deficits in ADHD

AU - Burwell, Scott J.

AU - Makeig, Scott

AU - Iacono, William G.

AU - Malone, Stephen M.

N1 - Funding Information: This research was made possible by funding from grant number AA017314 from the National Institute of Alcohol Abuse and Alcoholism (NIAAA) as well as grant numbers DA036216 and DA05147 from the National Institute on Drug Abuse (NIDA). In addition, SJB is funded by a NIDA T32 postdoctoral fellowship (DA037183) and received funding from the Society for Psychophysiological Research that enabled mentorship from SM at the Swartz Center for Computational Neuroscience (SCCN) at UCSD. SJB would like to acknowledge Shelby Piepho for assistance with manual preprocessing of structural MRI images as part of an undergraduate research experience. Also, SJB would like to thank Dr. Zeynep Akalin Acar and Matthew Burns at the SCCN for providing feedback in computational head modeling and regression ERP procedures, respectively, as well as Dr. Philip Burton at UMN's Center for Magnetic Resonance Research for his expert guidance in the cross-subject dipole coregistration method. SM's participation was funded by a gift from The Swartz Foundation (Old Field, NY). Publisher Copyright: © 2019 Society for Psychophysiological Research

PY - 2019

Y1 - 2019

N2 - Brain mechanisms linked to incorrect response selections made under time pressure during cognitive task performance are poorly understood, particularly in adolescents with attention-deficit hyperactivity disorder (ADHD). Using subject-specific multimodal imaging (electroencephalogram, magnetic resonance imaging, behavior) during flanker task performance by a sample of 94 human adolescents (mean age = 15.5 years, 50% female) with varying degrees of ADHD symptomatology, we examined the degree to which amplitude features of source-resolved event-related potentials (ERPs) from brain-independent component processes within a critical (but often ignored) period in the action selection process, the stimulus-response interval, were associated with motor response errors (across trials) and error rates (across individuals). Response errors were typically preceded by two smaller peaks in both trial-level and trial-averaged ERP projections from posterior medial frontal cortex (pMFC): a frontocentral P3 peaking about 390 ms after stimulus onset, and a premovement positivity (PMP) peaking about 110 ms before the motor response. Separating overlapping stimulus-locked and response-locked ERP contributions using a “regression ERP” approach showed that trial errors and participant error rates were primarily associated with smaller PMP, and not with frontocentral P3. Moreover, smaller PMP mediated the association between larger numbers of errors and ADHD symptoms, suggesting the possible value of using PMP as an intervention target to remediate performance deficits in ADHD.

AB - Brain mechanisms linked to incorrect response selections made under time pressure during cognitive task performance are poorly understood, particularly in adolescents with attention-deficit hyperactivity disorder (ADHD). Using subject-specific multimodal imaging (electroencephalogram, magnetic resonance imaging, behavior) during flanker task performance by a sample of 94 human adolescents (mean age = 15.5 years, 50% female) with varying degrees of ADHD symptomatology, we examined the degree to which amplitude features of source-resolved event-related potentials (ERPs) from brain-independent component processes within a critical (but often ignored) period in the action selection process, the stimulus-response interval, were associated with motor response errors (across trials) and error rates (across individuals). Response errors were typically preceded by two smaller peaks in both trial-level and trial-averaged ERP projections from posterior medial frontal cortex (pMFC): a frontocentral P3 peaking about 390 ms after stimulus onset, and a premovement positivity (PMP) peaking about 110 ms before the motor response. Separating overlapping stimulus-locked and response-locked ERP contributions using a “regression ERP” approach showed that trial errors and participant error rates were primarily associated with smaller PMP, and not with frontocentral P3. Moreover, smaller PMP mediated the association between larger numbers of errors and ADHD symptoms, suggesting the possible value of using PMP as an intervention target to remediate performance deficits in ADHD.

KW - ADHD

KW - ERP

KW - medial frontal cortex

KW - performance monitoring

KW - premovement positivity

KW - stimulus-response interval

UR - http://www.scopus.com/inward/record.url?scp=85065762720&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85065762720&partnerID=8YFLogxK

U2 - 10.1111/psyp.13392

DO - 10.1111/psyp.13392

M3 - Article

C2 - 31081153

AN - SCOPUS:85065762720

VL - 56

JO - Psychophysiology

JF - Psychophysiology

SN - 0048-5772

IS - 9

M1 - e13392

ER -

Reduced premovement positivity during the stimulus-response interval precedes errors: Using single-trial and regression ERPs to understand performance deficits in ADHD

Abstract

Bibliographical note

Keywords

Publisher link

Find It

Other files and links

Fingerprint

Cite this