Nucleus Accumbens Response to Reward Among Children with a Family History of Alcohol Use Problems: Convergent Findings from the ABCD Study and Michigan Longitudinal Study

Overview

Journal Brain Sci

Publisher MDPI

Date 2022 Jul 27

PMID 35884720

Authors

Meghan E Martz

Jillian E Hardee

Lora M Cope

Katherine L McCurry

Mary Soules

Robert A Zucker

Mary M Heitzeg

Affiliations

Soon will be listed here.

Abstract

Having a family history of alcohol use problems (FH+) conveys risk for alcohol use in offspring. Reward-related brain functioning may play a role in this vulnerability. The present study investigated brain function in the nucleus accumbens (NAcc) associated with the anticipation of reward in youth with two biological parents with alcohol use problems (FH+2), one biological parent with alcohol use problems (FH+1), and no biological parents with alcohol use problems (FH-). Participants were from the large, national Adolescent Brain Cognitive Development (ABCD) Study (mean age: 9.93; 48% female; FH+2 n = 223, FH+1 n = 1447, FH- n = 9690) and the Michigan Longitudinal Study (MLS), consisting of community-recruited families with high rates of alcohol use disorder (mean age: 10.54; 39.3% female; FH+2 n = 40, FH+1 n = 51, FH- n = 40). Reward anticipation was measured by the monetary incentive delay task. Regression models were used to assess associations between FH status and the anticipation of large rewards in right and left NAcc regions of interest. In both studies, FH+2 youth showed blunted anticipatory reward responding in the right NAcc compared to FH+1 youth. In the MLS, FH+2 youth also had blunted anticipatory reward responding in the right NAcc compared to the FH- group. Convergent results across two separate samples provide insights into a unique vulnerability of FH+2 youth and suggest that binary FH+ versus FH- categorizations may obscure important differences within FH+ youth.

Citing Articles

The ABCD and HBCD Studies: Longitudinal Studies to Inform Prevention Science.

Dowling G, Hoffman E, Cole K, Wargo E, Volkow N Focus (Am Psychiatr Publ). 2024; 22(4):449-457.

PMID: 39563872 PMC: 11571182. DOI: 10.1176/appi.focus.20240016.

How adverse childhood experiences get under the skin: A systematic review, integration and methodological discussion on threat and reward learning mechanisms.

Ruge J, Ehlers M, Kastrinogiannis A, Klingelhofer-Jens M, Koppold A, Abend R Elife. 2024; 13.

PMID: 39012794 PMC: 11251725. DOI: 10.7554/eLife.92700.

Neural responses to reward, threat, and emotion regulation and transition to hazardous alcohol use.

Kirk-Provencher K, Sloan M, Andereas K, Erickson C, Hakimi R, Penner A Alcohol Alcohol. 2024; 59(4).

PMID: 38953742 PMC: 11217988. DOI: 10.1093/alcalc/agae043.

Synaptic pruning during adolescence shapes adult social behavior in both males and females.

Kirkland J, Edgar E, Patel I, Feustel P, Belin S, Kopec A Dev Psychobiol. 2024; 66(3):e22473.

PMID: 38433422 PMC: 11758907. DOI: 10.1002/dev.22473.

Neural response to threat and reward among young adults at risk for alcohol use disorder.

Kirk-Provencher K, Hakimi R, Andereas K, Penner A, Gowin J Addict Biol. 2024; 29(2):e13378.

PMID: 38334006 PMC: 10898840. DOI: 10.1111/adb.13378.

References

Brislin S, Martz M, Joshi S, Duval E, Gard A, Clark D . Differentiated nomological networks of internalizing, externalizing, and the general factor of psychopathology (' factor') in emerging adolescence in the ABCD study. Psychol Med. 2021; 52(14):3051-3061. PMC: 9693677. DOI: 10.1017/S0033291720005103. View

Martz M, Zucker R, Schulenberg J, Heitzeg M . Psychosocial and neural indicators of resilience among youth with a family history of substance use disorder. Drug Alcohol Depend. 2018; 185:198-206. PMC: 5889747. DOI: 10.1016/j.drugalcdep.2017.12.015. View

Cope L, Martz M, Hardee J, Zucker R, Heitzeg M . Reward activation in childhood predicts adolescent substance use initiation in a high-risk sample. Drug Alcohol Depend. 2018; 194:318-325. PMC: 6540995. DOI: 10.1016/j.drugalcdep.2018.11.003. View

Paraskevopoulou M, van Rooij D, Schene A, Batalla A, Chauvin R, Buitelaar J . Effects of family history of substance use disorder on reward processing in adolescents with and without attention-deficit/hyperactivity disorder. Addict Biol. 2022; 27(2):e13137. PMC: 9285350. DOI: 10.1111/adb.13137. View

Zucker R . Genes, brain, behavior, and context: the developmental matrix of addictive behavior. Nebr Symp Motiv. 2014; 61:51-69. DOI: 10.1007/978-1-4939-0653-6_4. View

Knutson B, Westdorp A, Kaiser E, Hommer D . FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage. 2000; 12(1):20-7. DOI: 10.1006/nimg.2000.0593. View

Andrews M, Meda S, Thomas A, Potenza M, Krystal J, Worhunsky P . Individuals family history positive for alcoholism show functional magnetic resonance imaging differences in reward sensitivity that are related to impulsivity factors. Biol Psychiatry. 2010; 69(7):675-83. PMC: 3677031. DOI: 10.1016/j.biopsych.2010.09.049. View

Garavan H, Bartsch H, Conway K, Decastro A, Goldstein R, Heeringa S . Recruiting the ABCD sample: Design considerations and procedures. Dev Cogn Neurosci. 2018; 32:16-22. PMC: 6314286. DOI: 10.1016/j.dcn.2018.04.004. View

Stice E, Yokum S . Brain reward region responsivity of adolescents with and without parental substance use disorders. Psychol Addict Behav. 2013; 28(3):805-15. PMC: 3986351. DOI: 10.1037/a0034460. View

10.

Yau W, Zubieta J, Weiland B, Samudra P, Zucker R, Heitzeg M . Nucleus accumbens response to incentive stimuli anticipation in children of alcoholics: relationships with precursive behavioral risk and lifetime alcohol use. J Neurosci. 2012; 32(7):2544-51. PMC: 3567451. DOI: 10.1523/JNEUROSCI.1390-11.2012. View

11.

Lees B, Aguinaldo L, Squeglia L, Infante M, Wade N, Hernandez Mejia M . Parental Family History of Alcohol Use Disorder and Neural Correlates of Response Inhibition in Children From the Adolescent Brain Cognitive Development (ABCD) Study. Alcohol Clin Exp Res. 2020; 44(6):1234-1244. PMC: 7323844. DOI: 10.1111/acer.14343. View

12.

Muller K, Gan G, Banaschewski T, Barker G, Bokde A, Buchel C . No differences in ventral striatum responsivity between adolescents with a positive family history of alcoholism and controls. Addict Biol. 2014; 20(3):534-45. DOI: 10.1111/adb.12136. View

13.

Bjork J, Knutson B, Hommer D . Incentive-elicited striatal activation in adolescent children of alcoholics. Addiction. 2008; 103(8):1308-19. DOI: 10.1111/j.1360-0443.2008.02250.x. View

14.

Volkow N, Koob G, Croyle R, Bianchi D, Gordon J, Koroshetz W . The conception of the ABCD study: From substance use to a broad NIH collaboration. Dev Cogn Neurosci. 2017; 32:4-7. PMC: 5893417. DOI: 10.1016/j.dcn.2017.10.002. View

15.

Kwarteng A, Rahman M, Gee D, Infante M, Tapert S, Curtis B . Child reward neurocircuitry and parental substance use history: Findings from the Adolescent Brain Cognitive Development Study. Addict Behav. 2021; 122:107034. PMC: 8328938. DOI: 10.1016/j.addbeh.2021.107034. View

16.

Volkow N, Wise R, Baler R . The dopamine motive system: implications for drug and food addiction. Nat Rev Neurosci. 2017; 18(12):741-752. DOI: 10.1038/nrn.2017.130. View

17.

Greer S, Trujillo A, Glover G, Knutson B . Control of nucleus accumbens activity with neurofeedback. Neuroimage. 2014; 96:237-44. PMC: 4181613. DOI: 10.1016/j.neuroimage.2014.03.073. View

18.

Barnard M, McKeganey N . The impact of parental problem drug use on children: what is the problem and what can be done to help?. Addiction. 2004; 99(5):552-9. DOI: 10.1111/j.1360-0443.2003.00664.x. View

19.

Casey B, Cannonier T, Conley M, Cohen A, Barch D, Heitzeg M . The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites. Dev Cogn Neurosci. 2018; 32:43-54. PMC: 5999559. DOI: 10.1016/j.dcn.2018.03.001. View

20.

Wong M, Nigg J, Zucker R, Puttler L, Fitzgerald H, Jester J . Behavioral control and resiliency in the onset of alcohol and illicit drug use: a prospective study from preschool to adolescence. Child Dev. 2006; 77(4):1016-33. PMC: 2291361. DOI: 10.1111/j.1467-8624.2006.00916.x. View