Reward processing deficits and impulsivity in high-risk offspring of alcoholics: A study of event-related potentials during a monetary gambling task.

paper Primary Public

Authors: Kamarajan, Chella; Pandey, Ashwini K; Chorlian, David B; Manz, Niklas; Stimus, Arthur T; Bauer, Lance O; Hesselbrock, Victor M; Schuckit, Marc A; Kuperman, Samuel; Kramer, John; Porjesz, Bernice
Year: 2015
Journal: International journal of psychophysiology : official journal of the International Organization of Psychophysiology
PMID: 26388585
DOI: 10.1016/j.ijpsycho.2015.09.005
PMCID: PMC4898464

BACKGROUND: Individuals at high risk to develop alcoholism often manifest neurocognitive deficits as well as increased impulsivity. The goal of the present study is to elucidate reward processing deficits, externalizing disorders, and impulsivity as elicited by electrophysiological, clinical and behavioral measures in subjects at high risk for alcoholism from families densely affected by alcoholism in the context of brain maturation across age groups and gender. METHODS: Event-related potentials (ERPs) and current source density (CSD) during a monetary gambling task (MGT) were measured in 12-25 year old offspring (N=1864) of families in the Collaborative Study on the Genetics of Alcoholism (COGA) Prospective study; the high risk (HR, N=1569) subjects were from families densely affected with alcoholism and the low risk (LR, N=295) subjects were from community families. Externalizing disorders and impulsivity scores were also compared between LR and HR groups. RESULTS: HR offspring from older (16-25 years) male and younger (12-15 years) female subgroups showed lower P3 amplitude than LR subjects. The amplitude decrement was most prominent in HR males during the loss condition. Overall, P3 amplitude increase at anterior sites and decrease at posterior areas were seen in older compared to younger subjects, suggesting frontalization during brain maturation. The HR subgroups also exhibited hypofrontality manifested as weaker CSD activity during both loss and gain conditions at frontal regions. Further, the HR subjects had higher impulsivity scores and increased prevalence of externalizing disorders. P3 amplitudes during the gain condition were negatively correlated with impulsivity scores. CONCLUSIONS: Older male and younger female HR offspring, compared to their LR counterparts, manifested reward processing deficits as indexed by lower P3 amplitude and weaker CSD activity, along with higher prevalence of externalizing disorders and higher impulsivity scores. SIGNIFICANCE: Reward related P3 is a valuable measure reflecting neurocognitive dysfunction in subjects at risk for alcoholism, as well as to characterize reward processing and brain maturation across gender and age group.

Fig. 1

Schematic illustration of the monetary gambling task. Each trial starts with a choice stimulus (CS) which lasts for 800 ms and displays two amounts (10¢ or 50¢) to bet with. The participant selects one of the amounts and receives an outcome of either gain (green box) or loss (red box) for the selected amount as shown by the outcome stimulus (OS). A trial with a gain of 50¢ and the next trial with a loss of 10¢ are illustrated.

Fig. 2

Sixty-one electrodes as recorded in the current study from the surface of the scalp. Twelve electrodes (F3, FZ, F4, C3, CZ, C4, P3, PZ, P4, O1, OZ, O2) representing frontal, central, parietal and occipital regions were selected for statistical analyses.

Fig. 3

Qualitative comparison of mean P3 values for each subgroup during loss and gain conditions across 12 electrodes representing 4 regions (frontal: F3, FZ, F4; central: C3, CZ, C4; parietal: P3, PZ, P4; occipital: O1, OZ, O2). HR offspring display markedly lower P3 amplitude than LR subjects in both younger and older male subgroups during loss condition as well as in younger female subjects during both loss and gain conditions.

Fig. 4

Multiple comparisons across different groups during loss and gain conditions. Estimated marginal means and standard error (±1 SE) of pairwise comparisons between the levels of risk groups (panel-sets A1 and A2), gender (panel-sets B1 and B2), and age groups (panel-sets C1 and C2) in loss and gain condition have been plotted for each scalp region (F: frontal; C: central; P: parietal; and O: occipital). Bonferroni adjusted level of significance for each comparison is shown in asterisks (*p < 0.05, **p < 0.01, ***p < 0.001).

Fig. 5

Topographic maps and waveforms showing significant difference in P3 amplitude between HR and LR subjects in older males (panel A) and younger females (panel B) during the loss condition. The vertical dotted line in the waveform plots (middle subpanels) represents the onset of outcome stimulus, and the horizontal dashed line indicates the baseline (0 μV). The color scales for the topographic maps (left and right subpanels) represent P3 amplitude in μV.

Fig. 6

Topographic maps of CSD activity [panels A1, A2, B1, B2], and Z-scores [panels C1, C2, D2, D2]. Lower CSD activations of frontal sources and sinks are seen in HR offspring (more prominently among males) than LR group. Z-score maps are shown to highlight the topographic patterns more clearly across the different groups, but the magnitudes between the Z-score maps cannot be compared.

Fig. 7

Comparison of BIS scores between LR and HR subjects across subgroups and all subjects. HR offspring in each subgroup showed increased impulsivity in the BIS subscales and the total score. Error bars represent 1 standard deviation. Significance level for each comparison is shown by asterisks (*p < 0.05, **p < 0.01, ***p < 0.001).

#	Section	Preview
20	2. Materials and Methods — 2.4. EEG Data Acquisition and Signal Analysis	as well as for the gain condition (gain 10¢ + gain 50¢) in order to have more trials per subject…
21	2. Materials and Methods — 2.5. Current Source Density mapping	The recorded EEG potential at each electrode does not represent brain sources solely adjacent to the…
22	2. Materials and Methods — 2.5. Current Source Density mapping	spatially enhanced representation of current generators with more sharply localized peaks than those…
23	2. Materials and Methods — 2.5. Current Source Density mapping	described by Wang and Begleiter (1999). Z-scored maps for P3 amplitude as well as CSD were plotted…
24	2. Materials and Methods — 2.6. Statistical Analyses	Statistical analyses were performed using SPSS 21.0 (IBM Corporation, Armonk, NY). Prevalence rates…
25	2. Materials and Methods — 2.6. Statistical Analyses	Although affected status (i.e., individuals with any externalizing diagnosis as shown in Table 2)…
26	3. Results — 3.1. Prevalence Rates of Externalizing Disorders	Table 2 shows comparison of prevalence rates of externalizing (EXT) disorders, which includes DSM-IV…
27	3. Results — 3.2. Mean P3 Values across the Subgroups	Qualitative comparison of mean P3 values for each subgroup during loss and gain conditions are…
28	3. Results — 3.3. RM-ANOVA Results	Table 3 lists the main and interaction effects in the RM-ANOVA model, and Fig. 4 illustrates the…
29	3. Results — 3.3. RM-ANOVA Results — 3.3.1. Risk Group	A higher order interaction (risk group × condition × region) was found for risk group, suggesting…
30	3. Results — 3.3. RM-ANOVA Results — 3.3.2. Gender	In terms of gender effects, the 3-way interaction gender × condition × region interaction revealed…
31	3. Results — 3.3. RM-ANOVA Results — 3.3.3. Age Group	The age group × gender effect showed that younger male subjects manifested significantly higher P3…
32	3. Results — 3.3. RM-ANOVA Results — 3.3.4. Within-Subjects Factors	Effects of within-subjects factors (condition × region, condition, and region) were highly…
33	3. Results — 3.4. Current Source Density	Topographic maps of CSD for each subgroup during loss and gain conditions are shown in Fig. 6…
34	3. Results — 3.5. BIS Impulsivity — 3.5.1. Impulsivity Scores between LR and HR Subjects	Comparisons of impulsivity scores between LR and HR groups are shown in Fig. 7. Overall, in the…
35	3. Results — 3.5. BIS Impulsivity — 3.5.1. Impulsivity Scores between LR and HR Subjects	offspring had significantly higher impulsivity on all the scores than the LR subjects: non-planning…
36	3. Results — 3.5. BIS Impulsivity — 3.5.2. Correlations between BIS scores and P3 amplitudes	The relationship between P3 amplitude and impulsivity has been summarized in Table 4. Gain-related…
37	4. Discussion	The goal of the present study was to elucidate reward processing deficits as indexed by P3 amplitude…
38	4. Discussion — 4.1. P3 Deficits and Risk for Alcoholism — 4.1.1. P3, Cognitive Function and Reward Processing	In the current study, HR older male and younger female subgroups exhibited significantly lower P3…
39	4. Discussion — 4.1. P3 Deficits and Risk for Alcoholism — 4.1.2. Lower P3 in HR offspring	The major finding of the present study was that older male HR offspring and younger female HR…

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In this knowledge base

Title	Year	PMID
Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells?	2018	29897633
A KCNJ6 gene polymorphism modulates theta oscillations during reward processing.	2017	27993610

External

Title	Authors	Journal	Year	Link
Adverse childhood experiences as predictors of alcohol and tobacco addiction risk among college students in Delhi-NCR, India.	Chaudhary V et al.	—	2025	→
Effects of Alcohol on EEG Activity: A Systematic Review Focused on Sex-Related Differences in Youth.	Elliott AS et al.	—	2025	→
Characteristics of Adolescents with and without a Family History of Substance Use Disorder from a Minority Cohort.	Cheslack-Postava K et al.	—	2024	→
Feedback negativity and feedback-related P3 in individuals at risk for depression: Comparing surface potentials and current source densities.	Gao Y et al.	—	2024	→
Parental Deprivation- and Threat-Based Factors Associated with Youth Emotion-Based Neurocircuitry and Externalizing Behavior: A Systematic Review.	Feeney K et al.	—	2024	→
Family history of substance use disorder and likelihood of prescription drug misuse in adults 50 and older.	Schepis TS et al.	—	2023	→
The collaborative study on the genetics of alcoholism: Brain function.	Meyers JL et al.	—	2023	→
Serotonin 1B receptor effects on response inhibition are independent of inhibitory learning.	Desrochers SS et al.	—	2022	→
The Personality Traits and P300 of Offspring of Parents With Alcohol Dependence Differ Depending on Current Risky Drinking: A Preliminary Case-Control Study.	Qiu Y et al.	—	2022	→
A role for reward valuation in the serotonergic modulation of impulsivity.	Desrochers SS et al.	—	2021	→
It is all relative: Contextual influences on boredom and neural correlates of regulatory processes.	Perone S et al.	—	2021	→
Altered Reward Processing System in Internet Gaming Disorder.	Raiha S et al.	—	2020	→
Neuropsychophysiological Measures of Alcohol Dependence: Can We Use EEG in the Clinical Assessment?	Jurado-Barba R et al.	—	2020	→
Response Activation and Inhibition in Patients With Prolactinomas: An Electrophysiological Study.	Song J et al.	—	2020	→
Decision- and feedback-related brain potentials reveal risk processing mechanisms in patients with alcohol use disorder.	Sehrig S et al.	—	2019	→
Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells?	Prytkova I et al.	—	2018	→
Influence of socio-cultural factors on the emotional problems among college going young-adult children of parents with alcoholism: A study from South India.	Hebbani S et al.	—	2018	→
P3 Component as a Potential Endophenotype for Control Inhibition in Offspring of Alcoholics.	Domínguez-Centeno I et al.	—	2018	→
Reward-Based Learning as a Function of Severity of Substance Abuse Risk in Drug-Naïve Youth with ADHD.	Parvaz MA et al.	—	2018	→
Selective breeding for high alcohol consumption and response to nicotine: locomotor activity, dopaminergic in the mesolimbic system, and innate genetic differences in male and female alcohol-preferring, non-preferring, and replicate lines of high-alcohol drinking and low-alcohol drinking rats.	Deehan GA et al.	—	2018	→
A KCNJ6 gene polymorphism modulates theta oscillations during reward processing.	Kamarajan C et al.	—	2017	→
New Perspectives in the Exploration of Korsakoff's Syndrome: The Usefulness of Neurophysiological Markers.	Brion M et al.	—	2016	→
Deficient Event-Related Theta Oscillations in Individuals at Risk for Alcoholism: A Study of Reward Processing and Impulsivity Features.	Kamarajan C et al.	—	2015	→