Target-related parietal P3 and medial frontal theta index the genetic risk for problematic substance use

Jeremy Harper; Stephen M. Malone; William G. Iacono

doi:10.1111/psyp.13383

Target-related parietal P3 and medial frontal theta index the genetic risk for problematic substance use

Jeremy Harper, Stephen M. Malone, William G. Iacono

Psychology (Twin Cities)

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

Abstract

Theoretical and empirical work suggests that problematic substance use (PSU) is associated with individual differences in prefrontal cortex activity. While research has strongly linked parietal P3 amplitude reduction (P3AR) to genetic risk for problematic substance use, few studies have tested whether prefrontal EEG measures are sensitive to this genetic liability. In addition to P3, oddball target detection tasks elicit medial frontal theta power, reflecting attentional allocation, and parietal delta, indexing decision making or stimulus-response link updating. Midfrontal theta and parietal delta may index neurocognitive processes relevant to PSU beyond P3AR. The present investigation examined the etiological relationship between PSU and P3, frontal theta, and parietal delta in a large twin sample (N = 754). EEG was recorded during a visual oddball task. Greater PSU was associated with reduced target P3 amplitude and midfrontal theta/parietal delta power, and increased mean reaction time and reaction time variability (RTV; indexing attentional fluctuations). P3, theta, and RTV, but not delta or mean RT, explained unique variance in PSU (R² = 0.04). Twin biometric modeling indicated a genetic relationship between PSU and P3, theta, and RTV. Theta accounted for distinct genetic variance in PSU beyond P3 and RTV. Together, 23% of the total additive genetic variance in PSU was explained by the three endophenotypes. Results replicate P3AR as an endophenotype and provide support for additional behavioral (RTV) and neurophysiological (midfrontal theta) endophenotypes of PSU. Reduced theta and greater RTV may reflect variations in a prefrontal attentional network that confers genetic risk for substance use problems.

Original language	English (US)
Article number	e13383
Journal	Psychophysiology
Volume	56
Issue number	8
DOIs	https://doi.org/10.1111/psyp.13383
State	Published - Aug 2019

Bibliographical note

Funding Information:
National Institutes of Health grants (DA013240, DA036216); National Science Foundation Graduate Research Fellowship grant (No. 00039202), University of Minnesota Eva O. Miller Fellowship (to J.H.)

Funding Information:
This work was supported by the National Institutes of Health grants DA013240 and DA036216. J. H. was supported by the National Science Foundation Graduate Research Fellowship under grant No. 00039202 and the University of Minnesota Eva O. Miller Fellowship. None of the authors has a potential conflict of interest to be disclosed.

Keywords

P3
endophenotype
problematic substance use
reaction time variability
theta

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Twin Study

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title = "Target-related parietal P3 and medial frontal theta index the genetic risk for problematic substance use",

abstract = "Theoretical and empirical work suggests that problematic substance use (PSU) is associated with individual differences in prefrontal cortex activity. While research has strongly linked parietal P3 amplitude reduction (P3AR) to genetic risk for problematic substance use, few studies have tested whether prefrontal EEG measures are sensitive to this genetic liability. In addition to P3, oddball target detection tasks elicit medial frontal theta power, reflecting attentional allocation, and parietal delta, indexing decision making or stimulus-response link updating. Midfrontal theta and parietal delta may index neurocognitive processes relevant to PSU beyond P3AR. The present investigation examined the etiological relationship between PSU and P3, frontal theta, and parietal delta in a large twin sample (N = 754). EEG was recorded during a visual oddball task. Greater PSU was associated with reduced target P3 amplitude and midfrontal theta/parietal delta power, and increased mean reaction time and reaction time variability (RTV; indexing attentional fluctuations). P3, theta, and RTV, but not delta or mean RT, explained unique variance in PSU (R2 = 0.04). Twin biometric modeling indicated a genetic relationship between PSU and P3, theta, and RTV. Theta accounted for distinct genetic variance in PSU beyond P3 and RTV. Together, 23% of the total additive genetic variance in PSU was explained by the three endophenotypes. Results replicate P3AR as an endophenotype and provide support for additional behavioral (RTV) and neurophysiological (midfrontal theta) endophenotypes of PSU. Reduced theta and greater RTV may reflect variations in a prefrontal attentional network that confers genetic risk for substance use problems.",

keywords = "P3, endophenotype, problematic substance use, reaction time variability, theta",

author = "Jeremy Harper and Malone, {Stephen M.} and Iacono, {William G.}",

note = "Funding Information: National Institutes of Health grants (DA013240, DA036216); National Science Foundation Graduate Research Fellowship grant (No. 00039202), University of Minnesota Eva O. Miller Fellowship (to J.H.) Funding Information: This work was supported by the National Institutes of Health grants DA013240 and DA036216. J. H. was supported by the National Science Foundation Graduate Research Fellowship under grant No. 00039202 and the University of Minnesota Eva O. Miller Fellowship. None of the authors has a potential conflict of interest to be disclosed.",

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N1 - Funding Information: National Institutes of Health grants (DA013240, DA036216); National Science Foundation Graduate Research Fellowship grant (No. 00039202), University of Minnesota Eva O. Miller Fellowship (to J.H.) Funding Information: This work was supported by the National Institutes of Health grants DA013240 and DA036216. J. H. was supported by the National Science Foundation Graduate Research Fellowship under grant No. 00039202 and the University of Minnesota Eva O. Miller Fellowship. None of the authors has a potential conflict of interest to be disclosed.

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N2 - Theoretical and empirical work suggests that problematic substance use (PSU) is associated with individual differences in prefrontal cortex activity. While research has strongly linked parietal P3 amplitude reduction (P3AR) to genetic risk for problematic substance use, few studies have tested whether prefrontal EEG measures are sensitive to this genetic liability. In addition to P3, oddball target detection tasks elicit medial frontal theta power, reflecting attentional allocation, and parietal delta, indexing decision making or stimulus-response link updating. Midfrontal theta and parietal delta may index neurocognitive processes relevant to PSU beyond P3AR. The present investigation examined the etiological relationship between PSU and P3, frontal theta, and parietal delta in a large twin sample (N = 754). EEG was recorded during a visual oddball task. Greater PSU was associated with reduced target P3 amplitude and midfrontal theta/parietal delta power, and increased mean reaction time and reaction time variability (RTV; indexing attentional fluctuations). P3, theta, and RTV, but not delta or mean RT, explained unique variance in PSU (R2 = 0.04). Twin biometric modeling indicated a genetic relationship between PSU and P3, theta, and RTV. Theta accounted for distinct genetic variance in PSU beyond P3 and RTV. Together, 23% of the total additive genetic variance in PSU was explained by the three endophenotypes. Results replicate P3AR as an endophenotype and provide support for additional behavioral (RTV) and neurophysiological (midfrontal theta) endophenotypes of PSU. Reduced theta and greater RTV may reflect variations in a prefrontal attentional network that confers genetic risk for substance use problems.

AB - Theoretical and empirical work suggests that problematic substance use (PSU) is associated with individual differences in prefrontal cortex activity. While research has strongly linked parietal P3 amplitude reduction (P3AR) to genetic risk for problematic substance use, few studies have tested whether prefrontal EEG measures are sensitive to this genetic liability. In addition to P3, oddball target detection tasks elicit medial frontal theta power, reflecting attentional allocation, and parietal delta, indexing decision making or stimulus-response link updating. Midfrontal theta and parietal delta may index neurocognitive processes relevant to PSU beyond P3AR. The present investigation examined the etiological relationship between PSU and P3, frontal theta, and parietal delta in a large twin sample (N = 754). EEG was recorded during a visual oddball task. Greater PSU was associated with reduced target P3 amplitude and midfrontal theta/parietal delta power, and increased mean reaction time and reaction time variability (RTV; indexing attentional fluctuations). P3, theta, and RTV, but not delta or mean RT, explained unique variance in PSU (R2 = 0.04). Twin biometric modeling indicated a genetic relationship between PSU and P3, theta, and RTV. Theta accounted for distinct genetic variance in PSU beyond P3 and RTV. Together, 23% of the total additive genetic variance in PSU was explained by the three endophenotypes. Results replicate P3AR as an endophenotype and provide support for additional behavioral (RTV) and neurophysiological (midfrontal theta) endophenotypes of PSU. Reduced theta and greater RTV may reflect variations in a prefrontal attentional network that confers genetic risk for substance use problems.

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