Alterations of resting state functional network connectivity in the brain of nicotine and alcohol users.
- Authors
- Vergara, Victor M; Liu, Jingyu; Claus, Eric D; Hutchison, Kent; Calhoun, Vince
- Year
- 2017
- Journal
- NeuroImage
- PMID
- 27864080
- DOI
- 10.1016/j.neuroimage.2016.11.012
- PMCID
- PMC5420342
Alcohol and nicotine intake result in neurological alterations at the circuit level. Resting state functional connectivity has shown great potential in identifying these alterations. However, current studies focus on specific seeds and leave out many brain regions where effects might exist. The present study uses a data driven technique for brain segmentation covering the whole brain. Functional magnetic-resonance-imaging (fMRI) data were collected from 188 subjects:51 non-substance consumption controls (CTR), 36 smoking-and-drinking subjects (SAD), 28 drinkers (DRN), and 73 smokers (SMK). Data were processed using group independent component analysis to derive resting state networks (RSN). The resting state functional network connectivity (rsFNC) was then calculated through correlation between time courses. One-way ANOVA tests were used to detect rsFNC differences among the four groups. A total of 50 ANOVA tests were significant after multi-comparison correction. Results delineate a general pattern of hypo-connectivity in the substance consumers. Precuneus, postcentral gyrus, insula and visual cortex were the main brain areas with rsFNC reduction suggesting reduced interoceptive awareness in drinkers. In addition, connectivity reduction between postcentral and one RSN covering right fusiform and lingual gyri showed significant association with severity of hazardous drinking. In smokers, connectivity changes agreed with the idea of a shift towards endogenous information processing, represented by the DMN. Hypo-connectivity between thalamus and putamen was observed in smokers. In contrast, the angular gyrus showed hyper-connectivity with the precuneus linked to smoking and significantly correlated with nicotine dependence severity. In spite of the presence of common effects, our results suggest that particular effects of alcohol and nicotine can be separated and identified. Results also suggest that concurrent use of both substances affects brain connectivity in a complex manner, requiring careful consideration of interaction effects.
Set of 39 RSNs considered in this work. The figure was obtained using the spatial t-maps of each RSN. This set has been selected from a gICA decomposition with 100 components. A total of 61 gICA components were discarded based on frequency spectrum, peak activation located outside grey matter areas and visual inspection. Peak activation coordinates can be found in Table.
Mean rsFNC matrices for each sample group. CTR and SMK matrices are very similar with very few differences difficult to identify. The DRN and SAD matrices exhibit stronger differences compared to CTR between VIS-SEN, VISSAL and SEN-PRE groups.
Histogram summarizing significant rsFNC differences. The Fisher r-to-z transformation was applied to all correlation values and the color scale was restricted to the range [β1 1]. Results were classified according to the significance found on the sample groups. In those driven by βSmoking and Drinkingβ either the SAD group was different from CTR or both DRN and SMK groups were different. Driven by Drinking: only DRN was different from CTR. Driven by Smoking: only SMK was different from CTR. Significance is presented in the black and white histograms on the right. In those, one of the groups is set as baseline or reference and labeled as (REF). Significant relationship with AUDIT is labeled as βAβ, with FTND as βFβ, and the interaction AUDIT-FTND as βAFβ.
Networks with significant rsFNC differences. In this figure, changes in rsFNC are compared with respect to controls. Blue dots indicate the position of RSNs where hypo-connectivity was observed. Hypo-connectivity is the most common observation among rsFNCs driven by βSmoking and Drinkingβ. Red dots designate RSNs with hyper-connectivity. Hyper-connected RSNs were found in rsFNC driven by βDrinkingβ alone and βSmokingβ alone. The yellow dots were use for the RSN pair where smokers had increased negative connectivity (anti-correlation), but the drinkers exhibited decreased negative connectivity.
| Name | Type |
|---|---|
| abstinence | phenotype |
| alcohol | phenotype |
| alcohol abuse | phenotype |
| alcohol dependence | phenotype |
| alcoholism | phenotype |
| alcohol relapse | phenotype |
| Alcohol Use | phenotype |
| Alcohol Use Disorder | phenotype |
| angular gyrus | anatomy |
| anterior cingulate cortex | anatomy |
| Attention enhancement local | phenotype |
| AUDIT | phenotype |
| auditory | anatomy |
| binge drinking | phenotype |
| bipolar disorder | phenotype |
| Brain injury local | phenotype |
| Brain-related medical problems local | phenotype |
| cerebellar vermis | anatomy |
| cerebellum | anatomy |
| chronic alcoholism | phenotype |
| cingulate cortex | anatomy |
| cocaine | phenotype |
| cognition | phenotype |
| Cognitive dysregulation local | phenotype |
| Cognitive improvement local | phenotype |
| Colorado Twin Registry | cohort |
| control | cohort |
| controls | cohort |
| Convenience sample local | cohort |
| Coordination dysregulation local | phenotype |
| craving | phenotype |
| CTR group local | cohort |
| CTR subjects local | cohort |
| default mode network | anatomy |
| Default network (DMN) local | anatomy |
| depression | phenotype |
| Disconnection syndrome local | phenotype |
| DMN | anatomy |
| DMN group local | anatomy |
| DMN-precuneus connectivity local | phenotype |
| dopamine | drug |
| Drinker local | cohort |
| drinkers | phenotype |
| drinking | phenotype |
| DRN local | cohort |
| DRN group local | cohort |
| DRN population local | cohort |
| drug dependence | phenotype |
| DSM-IV | phenotype |
| dual users local | cohort |
| DVARS method local | drug |
| ECN local | anatomy |
| ECN group local | anatomy |
| ecstasy | drug |
| Executive control brain region local | anatomy |
| executive function | phenotype |
| Executive function areas local | anatomy |
| executive functioning | phenotype |
| Existing studies local | cohort |
| Extra-striate local | anatomy |
| Fronto-cerebellar network local | anatomy |
| fronto-parietal network | anatomy |
| FTND | phenotype |
| FTND-AUDIT interaction local | phenotype |
| FTND score | phenotype |
| Functional network connectivity local | phenotype |
| fusiform gyrus | anatomy |
| GABAergic receptors local | drug |
| General disconnection local | phenotype |
| glutamate | drug |
| hazardous drinking | phenotype |
| Heschl's gyrus | anatomy |
| hyper-connectivity local | phenotype |
| Hyper-connectivity local | phenotype |
| hypo-connectivity local | phenotype |
| illicit drugs | phenotype |
| Impulsive Sensation Seeking local | phenotype |
| income | phenotype |
| inferior frontal gyrus | anatomy |
| inferior occipital gyrus | anatomy |
| inferior parietal lobule | anatomy |
| insula | anatomy |
| Interoceptive awareness local | phenotype |
| Interoceptive dysfunction local | phenotype |
| Intrinsic connectivity local | phenotype |
| L Angular-Precuneus rsFNC local | anatomy |
| Left angular gyrus local | anatomy |
| left inferior parietal lobule | anatomy |
| left middle occipital gyrus local | anatomy |
| L Fusiform/Lingual-Cuneus rsFNC local | anatomy |
| Lingual cortex | anatomy |
| lingual gyrus | anatomy |
| Lingual/Vermis local | anatomy |
| Lingual/Vermis network local | anatomy |
| lobule VIIa local | anatomy |
| Long-term alcohol abstinence local | cohort |
| marijuana | phenotype |
| Memory enhancement local | phenotype |
| methamphetamine | drug |
| middle frontal gyrus | anatomy |
| middle occipital gyrus | anatomy |
| middle temporal gyrus | anatomy |
| Mild deficits local | phenotype |
| MNI standard space local | anatomy |
| Motor dysregulation local | phenotype |
| Motor enhancement local | phenotype |
| network dysfunction | phenotype |
| network global efficiency local | phenotype |
| Neurocognitive deficits | phenotype |
| never smokers | phenotype |
| nicotine | drug |
| nicotine addiction | phenotype |
| Nicotine craving behavior local | phenotype |
| nicotine dependence | phenotype |
| nicotine replacement therapy | drug |
| nicotine-seeking behavior local | phenotype |
| nicotine withdrawal | phenotype |
| normal controls | cohort |
| occipital gyrus local | anatomy |
| parietal cortex | anatomy |
| PCC | anatomy |
| Postcentral-3b local | anatomy |
| Postcentral-3b-R Fusiform Gyrus/Lingual rsFNC local | anatomy |
| postcentral gyrus | anatomy |
| Post-central gyrus local | anatomy |
| posterior cingulate cortex | anatomy |
| Precentral-3b local | anatomy |
| precentral gyrus | anatomy |
| precuneus | anatomy |
| PRE group local | anatomy |
| Prescription pain medication local | drug |
| primary visual cortex | anatomy |
| Primary visual region local | anatomy |
| Profound memory and abstract processing impairments local | phenotype |
| Protective effect local | phenotype |
| psychosis | phenotype |
| putamen | anatomy |
| Reduced awareness of input signals local | phenotype |
| Reduced connectivity local | phenotype |
| relapse | phenotype |
| Resting state functional connectivity local | phenotype |
| Resting state functional MRI local | drug |
| Resting state network local | anatomy |
| Resting State Network local | anatomy |
| Resting State Network (RSN) local | anatomy |
| Reward brain region local | anatomy |
| reward system | anatomy |
| right cuneus | anatomy |
| right inferior occipital gyrus local | anatomy |
| right superior occipital gyrus local | anatomy |
| rsFNC local | anatomy |
| rsFNC local | phenotype |
| rsFNC_Postcentral-3b_PCC local | phenotype |
| SAD local | cohort |
| SAD group local | cohort |
| SAL local | anatomy |
| SAL group local | anatomy |
| Salience disruption local | phenotype |
| salience network | anatomy |
| salience RSNs local | anatomy |
| sedatives | drug |
| Seed local | anatomy |
| Sensorial dysfunction local | phenotype |
| sensorimotor | anatomy |
| Sensorimotor area local | anatomy |
| Sensorimotor brain region local | anatomy |
| sensorimotor region | anatomy |
| sensorimotor RSNs local | anatomy |
| Siemens TIM Trio local | drug |
| SMA-6-R IOG rsFNC local | anatomy |
| SMK local | cohort |
| SMK group local | cohort |
| smoking | phenotype |
| Smoking and drinking local | cohort |
| Smoking drinkers local | cohort |
| smoking status | phenotype |
| Social drinkers | phenotype |
| SPM local | drug |
| stimulants | drug |
| study cohort | cohort |
| Subcortical brain region local | anatomy |
| subcortical regions | anatomy |
| substance abuse | phenotype |
| substance dependence subjects local | cohort |
| superior occipital gyrus | anatomy |
| superior temporal gyrus | anatomy |
| supplementary motor area | anatomy |
| supramarginal gyrus | anatomy |
| thalamus | anatomy |
| Thalamus-Putamen rsFNC local | anatomy |
| ventral tegmental area | anatomy |
| VIS group local | anatomy |
| visual | anatomy |
| visual areas local | anatomy |
| Visual brain region local | anatomy |
| visual dysfunction local | phenotype |
| visual memory local | phenotype |
| visual network | anatomy |
| visual processing | phenotype |
| visual region | anatomy |
| visual rsFNC differences local | phenotype |
| visual RSNs local | anatomy |
| withdrawal effects | phenotype |
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