Resiliency in adolescents at high risk for substance abuse: flexible adaptation via subthalamic nucleus and linkage to drinking and drug use in early adulthood.
- Authors
- Weiland, Barbara J; Nigg, Joel T; Welsh, Robert C; Yau, Wai-Ying W; Zubieta, Jon-Kar; Zucker, Robert A; Heitzeg, Mary M
- Year
- 2012
- Journal
- Alcoholism, clinical and experimental research
- PMID
- 22587751
- DOI
- 10.1111/j.1530-0277.2012.01741.x
- PMCID
- PMC3412943
INTRODUCTION: The personality trait resiliency is the ability to flexibly adapt impulse control relative to contextual demand. Low resiliency has been linked to later alcohol/drug problems. The underlying psychological and neural mechanisms are unknown, but neurocomputational models suggested relations between resiliency and working memory. Cortical-striatal connectivity has been proposed to underlie adaptive switches between cautious and risky behaviors. METHODS: Working memory was probed in sixty-seven 18- to 22-year-olds from a larger community study of alcoholism, using the n-back task during functional magnetic resonance imaging. Functional connectivity between task-related regions was investigated with psychophysiological interaction analysis. Resiliency was measured in early teen years and related to early adulthood measures of drinking/drug use, task activation, and connectivity. Relationships with risk factors, including family history, age of drinking onset, and number of alcohol problems, were also investigated. RESULTS: Higher resiliency was related to lower levels of substance use, fewer alcohol problems, and better working memory performance. Whole-brain regression revealed resiliency negatively correlated with activation of subthalamic nucleus (STN) and pallidum during the n-back. High and Low resiliency quartile groups (n = 17 each) differed in coupling strength between STN and median cingulate cortex, a region of reduced activation during working memory. The high resiliency group had later onset of drinking, fewer alcohol problems, had used fewer illicit drugs, and were less likely to smoke cigarettes than their low resiliency counterparts. CONCLUSIONS: These findings suggest that resiliency in early adolescence may protect against alcohol problems and drug use, although the direction of this effect is currently unknown. This protective factor may relate to executive functioning as supported by the finding of a neural link shared between resiliency and working memory in basal ganglia structures. The STN, a key basal ganglia structure, may adaptively link flexible impulse control with cognitive processing, potentially modulating substance use outcomes.
Depiction of n-back working memory task showing correct responses for the 0-back and 2-back conditions. The 0-back response requires identifying the numeral currently presented while the 2-back response involves updating, temporarily maintaining and storing information to recall numbers previously seen.
Group whole-brain contrast maps for 2-back vs. 0-back contrast for working memory task, displayed at a threshold of p<0.05 FDR corrected and minimum cluster size of 10, coordinates in MNI space. Orange regions represent regions more activated during 2-back working memory relative to the 0-back task while blue regions reflect the opposite relationship.
A) STN and pallidum regions of interest with negative correlation with resiliency measures from whole-brain group analysis displayed at a threshold of p<0.005 and minimum cluster size of 50, coordinates in MNI space. B) Extracted bilateral pallidum and STN activity during 2-back vs. 0-back condition of working memory plotted against individual resiliency measures for all subjects (n=67).
A) Bilateral median cingulate regions with different connectivity between Low and High resiliency groups (n=17 each), displayed at a threshold of p<0.005, voxel extent = 25, coordinates in MNI space. B) Connectivity strength with right STN for bilateral median cingulate ROIs for Low (n=17), Mid (n=33) and High (n=17) Resiliency Groups for 2-back vs. 0-back working memory: left cingulate region was identified at more lenient threshold as shown above. The Low resiliency quartile exhibited positive connectivity defined as stronger functional connectivity between regions for 2-back vs. 0-back working memory, while the High resiliency had negative connectivity reflecting less functional connectivity between regions for 2-back vs. 0-back task. Error bars: ± 1 Standard Error.
| Name | Type |
|---|---|
| 0-back condition local | phenotype |
| 0-back RT local | phenotype |
| 2-back condition local | phenotype |
| 2-back PD local | phenotype |
| addiction | phenotype |
| adolescents | cohort |
| age of onset | phenotype |
| alcohol | phenotype |
| alcohol abuse | phenotype |
| alcohol dependence | phenotype |
| alcoholism | phenotype |
| Alcohol Problems | phenotype |
| alcohol-related outcomes | phenotype |
| anterior cingulate cortex | anatomy |
| attention deficit hyperactivity disorder | phenotype |
| axis I disorder | phenotype |
| basal ganglia | anatomy |
| behavioral measures | phenotype |
| Brodmann area 23 local | anatomy |
| Brodmann area 24 | anatomy |
| childhood | cohort |
| cigarettes | phenotype |
| cingulate cortex | anatomy |
| Cingulate region local | anatomy |
| cocaine | phenotype |
| Cognitive changes | phenotype |
| conduct disorder | phenotype |
| Default network region local | anatomy |
| developmental disorders | phenotype |
| Dopaminergic treatment local | drug |
| drinking | phenotype |
| drug dependence | phenotype |
| Drug use behaviors local | phenotype |
| early adulthood | cohort |
| early alcohol use | phenotype |
| Early use of substances local | phenotype |
| Excluded runs local | phenotype |
| executive function | phenotype |
| executive functioning | phenotype |
| externalizing disorders | phenotype |
| familial risk | cohort |
| family history group local | cohort |
| family history negative | phenotype |
| family history positive | phenotype |
| FH+ | drug |
| FHN | cohort |
| FH+ subjects | cohort |
| food intake | phenotype |
| frontal cortex | anatomy |
| heavy drinking | phenotype |
| High-drinker rats local | cohort |
| High-quartile resiliency group local | cohort |
| High resiliency local | cohort |
| High resiliency local | phenotype |
| High resiliency group local | cohort |
| High resiliency quartile local | cohort |
| illicit drugs | phenotype |
| Illicit drugs used local | phenotype |
| illicit drug use | phenotype |
| impulsive action | phenotype |
| impulsive choice | phenotype |
| incentive salience | phenotype |
| inferior parietal lobe | anatomy |
| Intelligence quotient | phenotype |
| interference control local | phenotype |
| IQ | phenotype |
| left inferior frontal gyrus | anatomy |
| Left median cingulate local | anatomy |
| Left STN local | anatomy |
| limbic system | anatomy |
| Low-drinker rats local | cohort |
| Low-quartile resiliency group local | cohort |
| Low resiliency local | cohort |
| Low resiliency local | phenotype |
| Low resiliency group local | cohort |
| Low resiliency quartile local | cohort |
| medial frontal cortex | anatomy |
| median cingulate | anatomy |
| mid-adolescence | cohort |
| MLS | cohort |
| MLS population local | cohort |
| MLS sample local | cohort |
| MLS study local | cohort |
| motivation | phenotype |
| n-back task local | drug |
| Number of illicit drugs ever used local | phenotype |
| pallidum | anatomy |
| parental alcoholism | phenotype |
| parietal cortex | anatomy |
| Parkinson's disease local | cohort |
| Parkinson’s patients local | cohort |
| pathological gambling | phenotype |
| PD | phenotype |
| performance | phenotype |
| performance decrement local | phenotype |
| planning | phenotype |
| postcentral gyrus | anatomy |
| posterior cingulate cortex | anatomy |
| precentral gyrus | anatomy |
| prefrontal cortex | anatomy |
| processing speed | phenotype |
| psychosis | phenotype |
| reaction time | phenotype |
| regulatory trait resiliency local | phenotype |
| resiliency local | phenotype |
| Resiliency local | phenotype |
| resiliency group local | cohort |
| resiliency groups local | cohort |
| Resiliency Groups local | cohort |
| response inhibition | phenotype |
| response time | phenotype |
| right-handed youth local | cohort |
| right median cingulate local | anatomy |
| Right median cingulate (BA 23) local | anatomy |
| right prefrontal cortex | anatomy |
| right STN local | anatomy |
| Right STN local | anatomy |
| right STN-right median cingulate connectivity local | anatomy |
| RT | phenotype |
| schizophrenia | phenotype |
| seed ROIs local | anatomy |
| sex | phenotype |
| smoking | phenotype |
| STN | anatomy |
| Study cohort (n=67) local | cohort |
| subjects | cohort |
| substance abuse | phenotype |
| substance use | phenotype |
| substance use measures local | phenotype |
| subthalamic nucleus | anatomy |
| Total drinking local | phenotype |
| total drinking in the past six months local | phenotype |
| TRB factor 1 | phenotype |
| vulnerability | phenotype |
| vulnerability measures local | phenotype |
| whole brain | anatomy |
| working memory | phenotype |
| young adults | cohort |
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In this knowledge base
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|---|---|---|
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