Accumbens functional connectivity during reward mediates sensation-seeking and alcohol use in high-risk youth.

paper Cited Public

Authors: Weiland, Barbara J; Welsh, Robert C; Yau, Wai-Ying Wendy; Zucker, Robert A; Zubieta, Jon-Kar; Heitzeg, Mary M
Year: 2013
Journal: Drug and alcohol dependence
PMID: 22958950
DOI: 10.1016/j.drugalcdep.2012.08.019
PMCID: PMC3546225

BACKGROUND: Differences in fronto-striatal connectivity in problem substance users have suggested reduced influence of cognitive regions on reward-salience regions. Youth with a family history of alcoholism (FH+) have disrupted ventral striatal processing compared with controls with no familial risk (FH-). As sensation-seeking represents an additional vulnerability factor, we hypothesized that functional connectivity during reward anticipation would differ by family history, and would mediate the relationship between sensation-seeking and drinking in high-risk subjects. METHODS: Seventy 18-22 year olds (49 FH+/21 FH-) performed a monetary incentive delay task during functional magnetic resonance imaging. Group connectivity differences for incentive (reward/loss) vs. neutral conditions were evaluated with psychophysiological interaction (PPI) analysis, seeded in nucleus accumbens (NAcc). Indirect effects of sensation-seeking on drinking volume through accumbens connectivity were tested. RESULTS: NAcc connectivity with paracentral lobule/precuneus and sensorimotor areas was decreased for FH- vs. increased for FH+ during incentive anticipation. In FH+, task-related functional coupling between left NAcc and supplementary sensorimotor area (SSMA) and right precuneus correlated positively with sensation-seeking and drinking volume and mediated their relationship. In FH-, left NAcc-SSMA connectivity correlated negatively with sensation-seeking but was not related to drinking. CONCLUSIONS: These results suggest preexisting differences in accumbens reward-related functional connectivity in high-risk subjects. NAcc coupling with SSMA, involved in attention and motor networks, and precuneus, a default mode structure, appear to mediate sensation-seeking's effect on drinking in those most at-risk. Differences in accumbens connectivity with attention/motor/default networks, rather than control systems, may influence the reward system's role in vulnerability for substance abuse.

Figure 1

A) Schematic illustration of the monetary incentive delay task performed by subjects in the fMRI scanner. B) Location of 5-mm diameter spherical nucleus accumbens mask at the ventromesial intersection of caudate and putamen (y=13 MNI). C) Activation in bilateral nucleus accumbens during reward and loss anticipation by family history groups. Error bars: ± 1 Standard Error.

Figure 2

Regions with negative functional connectivity with NAcc during incentive including areas. FH− controls have reduced task connectivity in regions which map onto default mode network resting state regions representing areas significantly decoupled during incentive processing. A) Functional connectivity for FH− controls with left NAcc; B) functional connectivity for FH− controls with right NAcc; C) Functional connectivity for FH+ with left NAcc; D) functional connectivity for FH+ with right NAcc. Data are displayed on the lateral and medial surfaces of the left hemisphere (Left), the dorsal surface (Center), and the lateral and medial surfaces of the right hemisphere (Right) for each NAcc. Connectivity maps are displayed at cluster-level p<0.05 corrected with the exception of D) which is displayed at cluster-level p<0.08 due to lack of significant clusters at the more stringent threshold.

Figure 3

Extracted task-related functional connectivity change with NAcc during Incentive>Neutral anticipatory processing by family history group. L, left; R, right; NAcc, nucleus accumbens; SSMA, supplementary sensoriomotor area; PoG, postcentral gyrus; SMA, supplementary motor area; OCC, occipital.

Figure 4

A) Statistical parametric maps identifying large cluster designated supplementary sensorimotor area (SSMA). B) Correlations between left NAcc–SSMA incentive connectivity change and sensation-seeking by family history group. C) Correlations between left NAcc–SSMA incentive connectivity change and transformed drinking volume for the past six months by family history group.

Figure 5

Meditation model of vulnerability with unstandardized coefficients testing indirect effect of connectivity on relationship of sensation-seeking on drinking volume.

#	Section	Preview
40	4. DISCUSSION	This study found that functional connectivity with reward/salience regions, specifically the NAcc,…

Name	Type
Acute medical illness local	phenotype
addiction	phenotype
Addictive substance use local	phenotype
alcohol	phenotype
alcoholism	phenotype
alcoholism risk	phenotype
Alcohol Use	phenotype
amount	phenotype
amygdala	anatomy
anterior cingulate cortex	anatomy
anticipation of incentive stimuli local	phenotype
Anticipatory striatal activation local	anatomy
anxiety	phenotype
attention deficit hyperactivity disorder	phenotype
attention network	anatomy
auditory/phonology network local	anatomy
axis I disorder	phenotype
basal ganglia	anatomy
caudate nucleus	anatomy
Centrally active medications local	drug
cerebellum	anatomy
cerebral hemispheres	anatomy
Chronic health conditions	phenotype
chronic heroin users local	cohort
Cognitive control regions local	anatomy
conduct disorder	phenotype
connectivity change local	phenotype
control group	cohort
Control network local	anatomy
control subjects	cohort
cortex	anatomy
craving	phenotype
DD	phenotype
decision-making deficits	phenotype
default mode network	anatomy
depression	phenotype
DMN	anatomy
drinking	phenotype
drinking volume local	phenotype
Drinking volume local	phenotype
drug dependence	phenotype
DV	phenotype
early substance use	phenotype
externalizing disorders	phenotype
Familial liability local	phenotype
familial risk	cohort
familial risk for substance abuse local	phenotype
family history negative	phenotype
family history of alcoholism	phenotype
family history positive	phenotype
fetal alcohol syndrome	phenotype
FH	cohort
FH+	drug
FH− local	cohort
FH+ families local	cohort
FH− families local	cohort
FH group local	cohort
FHN	cohort
FH+ subjects	cohort
FH- subjects local	cohort
FH− subjects local	cohort
First 70 neuroimaging participants local	cohort
Food sensitivity local	phenotype
functional connectivity	phenotype
group	cohort
healthy controls	cohort
heavy drinking	phenotype
heroin users	phenotype
High-risk population local	cohort
high-risk subjects	cohort
High risk taking local	phenotype
hippocampus	anatomy
hostility	phenotype
Impulsive decision making	phenotype
incentive anticipation local	phenotype
incentive connectivity change local	phenotype
inferior parietal lobe	anatomy
inhibitory control deficits local	phenotype
insula	anatomy
lateral temporal lobe local	anatomy
left NAcc-right precuneus connectivity local	anatomy
Left NAcc-right precuneus connectivity local	phenotype
left NAcc-SSMA local	anatomy
Left NAcc-SSMA incentive connectivity local	phenotype
limbic regions	anatomy
loss	phenotype
loss anticipation	phenotype
low familial risk for substance abuse local	phenotype
medial orbitofrontal cortex	anatomy
medial prefrontal cortex	anatomy
medial SSMA local	anatomy
Michigan Longitudinal Study	cohort
midbrain	anatomy
Midline areas local	anatomy
midline regions	anatomy
MLS	cohort
motor network local	anatomy
Motor network local	anatomy
NAcc	anatomy
NAcc-SSMA connectivity local	anatomy
Neurological illness local	phenotype
neutral	phenotype
neutral condition	phenotype
Nonalcoholic families local	phenotype
novelty seeking	phenotype
nucleus accumbens	anatomy
obesity	phenotype
occipital cortex	anatomy
occipital regions local	anatomy
Occipital regions local	anatomy
orbitofrontal cortex	anatomy
other ROIs local	anatomy
overeating	phenotype
paracentral local	anatomy
paracentral lobule	anatomy
parental alcoholism	phenotype
parietal cortex	anatomy
participants	cohort
polysubstance abuse	phenotype
positive affect	phenotype
postcentral gyrus	anatomy
precentral gyrus	anatomy
precuneus	anatomy
premotor cortex	anatomy
problem substance users local	cohort
psychosis	phenotype
putamen	anatomy
reaction time	phenotype
regulation deficits local	phenotype
reward	phenotype
reward anticipation	phenotype
Reward‑related circuitry local	anatomy
Reward-related functional connectivity with the NAcc local	anatomy
reward system	anatomy
Reward task performance local	phenotype
right lingual gyrus	anatomy
right NAcc-SSMA local	anatomy
right NAcc-SSMA connectivity local	phenotype
Risk-related behaviors local	phenotype
saliency responses local	phenotype
schizophrenia	phenotype
sedatives	drug
self-referential network local	anatomy
Sensation‑seeking local	phenotype
sensation-seeking personality local	phenotype
sensation-seeking score local	phenotype
sensorimotor cortex	anatomy
striatum	anatomy
substance abuse	phenotype
substance-dependent subjects local	cohort
substance use	phenotype
substantia nigra	anatomy
success rate	phenotype
superior temporal local	anatomy
supplemental motor area local	anatomy
supplementary sensorimotor area local	anatomy
Supplementary sensorimotor area local	anatomy
Target duration local	phenotype
task difficulty	phenotype
temporal lobe	anatomy
valence	phenotype
ventral/rostral anterior cingulate local	anatomy
ventral striatum	anatomy
ventral tegmental area	anatomy
visual network	anatomy
young adults	cohort

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In this knowledge base

Title	Year	PMID
Random Forest Classification of Alcohol Use Disorder Using EEG Source Functional Connectivity, Neuropsychological Functioning, and Impulsivity Measures.	2020	32121585
Reward processing deficits and impulsivity in high-risk offspring of alcoholics: A study of event-related potentials during a monetary gambling task.	2015	26388585
Family history of alcohol use disorders and neuromaturation: a functional connectivity study with adolescents.	2013	24200205

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Striatal activation and frontostriatal connectivity during non-drug reward anticipation in alcohol dependence.	Becker A et al.	—	2017	→
Age associations with neural processing of reward anticipation in adolescents with bipolar disorders.	Urošević S et al.	—	2016	→
Modulation of meso-limbic reward processing by motivational tendencies in young adolescents and adults.	Joseph JE et al.	—	2016	→
Neurobiological phenotypes associated with a family history of alcoholism.	Cservenka A	—	2016	→
Nucleus accumbens functional connectivity discriminates medication-overuse headache.	Torta DM et al.	—	2016	→
Reduced Functional Connectivity within the Mesocorticolimbic System in Substance Use Disorders: An fMRI Study of Puerto Rican Young Adults.	Posner J et al.	—	2016	→
Reward Contingencies Improve Goal-Directed Behavior by Enhancing Posterior Brain Attentional Regions and Increasing Corticostriatal Connectivity in Cocaine Addicts.	Rosell-Negre P et al.	—	2016	→
Transdiagnostic commonalities and differences in resting state functional connectivity of the default mode network in schizophrenia and major depression.	Schilbach L et al.	—	2016	→
Winning is not enough: ventral striatum connectivity during physical aggression.	Buades-Rotger M et al.	—	2016	→
Advances in Human Neuroconnectivity Research: Applications for Understanding Familial History Risk for Alcoholism.	Cservenka A et al.	—	2015	→
Does incentive-elicited nucleus accumbens activation differ by substance of abuse? An examination with adolescents.	Karoly HC et al.	—	2015	→
Earlier adolescent substance use onset predicts stronger connectivity between reward and cognitive control brain networks.	Weissman DG et al.	—	2015	→
Early Life Stress, Nicotinic Acetylcholine Receptors and Alcohol Use Disorders.	Holgate JY et al.	—	2015	→
Family history density of alcoholism relates to left nucleus accumbens volume in adolescent girls.	Cservenka A et al.	—	2015	→
Influence of neurobehavioral incentive valence and magnitude on alcohol drinking behavior.	Joseph JE et al.	—	2015	→
National multi-cohort time trends in adolescent risk preference and the relation with substance use and problem behavior from 1976 to 2011.	Keyes KM et al.	—	2015	→
Neuroimaging Risk Markers for Substance Abuse: Recent Findings on Inhibitory Control and Reward System Functioning.	Heitzeg MM et al.	—	2015	→
Reward processing deficits and impulsivity in high-risk offspring of alcoholics: A study of event-related potentials during a monetary gambling task.	Kamarajan C et al.	—	2015	→
The association between alcohol, marijuana use, and new and emerging tobacco products in a young adult population.	Cohn A et al.	—	2015	→
The quality of adolescents' peer relationships modulates neural sensitivity to risk taking.	Telzer EH et al.	—	2015	→
Differential reward network functional connectivity in cannabis dependent and non-dependent users.	Filbey FM et al.	—	2014	→
Exploring the relationship of functional network connectivity to latent trajectories of alcohol use and risky sex.	Thayer RE et al.	—	2014	→
Functional connectivity in prenatally stressed rats with and without maternal treatment with ladostigil, a brain-selective monoamine oxidase inhibitor.	Goelman G et al.	—	2014	→
Mapping the development of the basal ganglia in children with attention-deficit/hyperactivity disorder.	Shaw P et al.	—	2014	→
Prefrontal response and frontostriatal functional connectivity to monetary reward in abstinent alcohol-dependent young adults.	Forbes EE et al.	—	2014	→
Relationship between impulsivity, prefrontal anticipatory activation, and striatal dopamine release during rewarded task performance.	Weiland BJ et al.	—	2014	→
Resting state functional connectivity of the nucleus accumbens in youth with a family history of alcoholism.	Cservenka A et al.	—	2014	→
Risk perception, motives and behaviours in university students.	Salameh P et al.	—	2014	→
Sweet-liking is associated with transformation of heavy drinking into alcohol-related problems in young adults with high novelty seeking.	Kampov-Polevoy A et al.	—	2014	→
Family history of alcohol use disorders and neuromaturation: a functional connectivity study with adolescents.	Spadoni AD et al.	—	2013	→
What is a representative brain? Neuroscience meets population science.	Falk EB et al.	—	2013	→