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      Alcoholism gender differences in brain responsivity to emotional stimuli

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          Abstract

          Men and women may use alcohol to regulate emotions differently, with corresponding differences in neural responses. We explored how the viewing of different types of emotionally salient stimuli impacted brain activity observed through functional magnetic resonance imaging (fMRI) from 42 long-term abstinent alcoholic (25 women) and 46 nonalcoholic (24 women) participants. Analyses revealed blunted brain responsivity in alcoholic compared to nonalcoholic groups, as well as gender differences in those activation patterns. Brain activation in alcoholic men (ALC M) was significantly lower than in nonalcoholic men (NC M) in regions including rostral middle and superior frontal cortex, precentral gyrus, and inferior parietal cortex, whereas activation was higher in alcoholic women (ALC W) than in nonalcoholic women (NC W) in superior frontal and supramarginal cortical regions. The reduced brain reactivity of ALC M, and increases for ALC W, highlighted divergent brain regions and gender effects, suggesting possible differences in the underlying basis for development of alcohol use disorders.

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          More than 100 million people worldwide are thought to have alcohol use disorder, also known as AUD, alcohol dependence or alcoholism. People who struggle to regulate their emotions tend to consume more alcohol than others. This suggests that impaired emotion processing may increase the risk of developing the disorder.

          Most studies of emotion processing in people with alcohol use disorder do not distinguish between men and women. But evidence suggests that men and women process emotions in different ways. Sawyer et al. set out to explore the possible relationships between emotion processing, gender and alcoholism. Four groups of volunteers took part in the study: abstinent men and women with the disorder, and control groups of men and women without a history of alcoholism. Each group contained between 15 and 21 participants. The two abstinent alcoholic groups had not consumed alcohol for at least 21 days. The average length of abstinence was 7 years.

          The volunteers viewed a mixture of emotionally charged and neutral images while lying inside a brain scanner. The emotionally charged images were of happy, erotic, gruesome or aversive scenes. Sawyer et al. measured the difference in brain responses to the emotionally charged images versus the neutral ones, and compared this measure across the four groups of participants. Abstinent alcoholic men showed muted brain responses to the emotionally charged images compared to their female counterparts. This effect was seen in brain regions involved in memory, emotion processing and social processing. The same pattern occurred for all four types of emotionally charged image.

          Abstinent alcoholic men also showed smaller brain responses to the emotionally charged images than non-alcoholic control men. By contrast, abstinent alcoholic women showed larger brain responses to the emotionally charged images than non-alcoholic control women. This suggests that abstinent alcoholic men and women differ in the way they process emotions. Future studies should investigate whether these differences emerge over the course of abstinence. They should also examine whether these differences might contribute to, or result from, differences in alcohol use disorder between men and women.

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          Most cited references61

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          Emotional processing in anterior cingulate and medial prefrontal cortex.

          Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions. Published by Elsevier Ltd.
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            Emotion, decision making and the orbitofrontal cortex.

            The somatic marker hypothesis provides a systems-level neuroanatomical and cognitive framework for decision making and the influence on it by emotion. The key idea of this hypothesis is that decision making is a process that is influenced by marker signals that arise in bioregulatory processes, including those that express themselves in emotions and feelings. This influence can occur at multiple levels of operation, some of which occur consciously and some of which occur non-consciously. Here we review studies that confirm various predictions from the hypothesis. The orbitofrontal cortex represents one critical structure in a neural system subserving decision making. Decision making is not mediated by the orbitofrontal cortex alone, but arises from large-scale systems that include other cortical and subcortical components. Such structures include the amygdala, the somatosensory/insular cortices and the peripheral nervous system. Here we focus only on the role of the orbitofrontal cortex in decision making and emotional processing, and the relationship between emotion, decision making and other cognitive functions of the frontal lobe, namely working memory.
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              Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epidemiologic Catchment Area (ECA) Study.

              The prevalence of comorbid alcohol, other drug, and mental disorders in the US total community and institutional population was determined from 20,291 persons interviewed in the National Institute of Mental Health Epidemiologic Catchment Area Program. Estimated US population lifetime prevalence rates were 22.5% for any non-substance abuse mental disorder, 13.5% for alcohol dependence-abuse, and 6.1% for other drug dependence-abuse. Among those with a mental disorder, the odds ratio of having some addictive disorder was 2.7, with a lifetime prevalence of about 29% (including an overlapping 22% with an alcohol and 15% with another drug disorder). For those with either an alcohol or other drug disorder, the odds of having the other addictive disorder were seven times greater than in the rest of the population. Among those with an alcohol disorder, 37% had a comorbid mental disorder. The highest mental-addictive disorder comorbidity rate was found for those with drug (other than alcohol) disorders, among whom more than half (53%) were found to have a mental disorder with an odds ratio of 4.5. Individuals treated in specialty mental health and addictive disorder clinical settings have significantly higher odds of having comorbid disorders. Among the institutional settings, comorbidity of addictive and severe mental disorders was highest in the prison population, most notably with antisocial personality, schizophrenia, and bipolar disorders.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                30 April 2019
                2019
                : 8
                : e41723
                Affiliations
                [1 ]deptPsychology Research Service VA Healthcare System BostonUnited States
                [2 ]deptDepartment of Anatomy and Neurobiology Boston University School of Medicine BostonUnited States
                [3 ]deptDepartment of Radiology Massachusetts General Hospital BostonUnited States
                [4 ]Sawyer Scientific, LLC BostonUnited States
                [5 ]deptDepartment of Psychiatry Massachusetts General Hospital BostonUnited States
                [6 ]deptDepartment of Psychology San Diego State University San DiegoUnited States
                [7 ]deptDepartment of Computer Science Dartmouth College HanoverUnited States
                [8 ]dept3D Imaging Service Massachusetts General Hospital BostonUnited States
                [9 ]deptDepartment of Psychiatry Boston University School of Medicine BostonUnited States
                [10 ]deptDepartment of Neurology Boston University School of Medicine BostonUnited States
                University of Florida United States
                University of Pennsylvania United States
                University of Florida United States
                Author information
                https://orcid.org/0000-0001-7767-5688
                https://orcid.org/0000-0003-1658-4496
                http://orcid.org/0000-0003-0100-8883
                Article
                41723
                10.7554/eLife.41723
                6491039
                31038125
                0de11ed8-49f4-4598-8e82-5b166ddd46fa

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 05 September 2018
                : 29 March 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000738, U.S. Department of Veterans Affairs;
                Award ID: I01CX000326
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000027, National Institute on Alcohol Abuse and Alcoholism;
                Award ID: R01AA07112
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001443, ABMRF/The Foundation for Alcohol Research;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000027, National Institute on Alcohol Abuse and Alcoholism;
                Award ID: R01AA016624
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000027, National Institute on Alcohol Abuse and Alcoholism;
                Award ID: K05AA00219
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000027, National Institute on Alcohol Abuse and Alcoholism;
                Award ID: K01AA13402
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Human Biology and Medicine
                Neuroscience
                Custom metadata
                Neuroimaging shows brain responses to emotional pictures are more diminished in alcoholic men than in alcoholic women, implicating gender-related mechanisms of addiction.

                Life sciences
                alcoholism,fmri,emotion,gender,sex,brain,human
                Life sciences
                alcoholism, fmri, emotion, gender, sex, brain, human

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