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Childhood Trauma, Emotional Awareness, and Neural Correlates of Long-Term Nicotine Smoking.

A figure from this studyHot Off the Press – January 30, 2024

Published in JAMA Network Open by Annika Quam and Amy Janes et al. from the NIDA IRP Cognitive and Pharmacological Neuroimaging Unit.

Summary

As a primary cause of preventable death, nicotine dependence remains a significant public health concern. While there are several medications that help people quit smoking, many individuals relapse despite receiving support. To suggest new directions for treatment, our lab works to understand how brain function and nicotine use are related. Here, we used an fMRI imaging technique called temporal dynamics, which allows us to measure brain function when someone is resting in the scanner. When comparing brain function between those who do and do not smoke, we found that individuals who do smoke spent more time in the frontoinsular default mode network (FI-DMN) state. This is relevant because engagement of FI-DMN brain regions has been linked with ruminating on how one feels, craving, and the maintenance of nicotine dependence. We show that even when someone is not doing anything, nicotine dependent individuals spend more time in a brain state linked with continued nicotine use. Moving a step further, we asked whether a history of childhood trauma and related emotion dysregulation would impact our results. This is important because childhood trauma exposure places one at risk for developing emotion dysregulation and substance use. We found that trauma-related emotion dysregulation, specifically when individuals have difficulty identifying and expressing emotions, was associated with spending less time in the FI-DMN. But, this was only true for those who use nicotine. While our group level results showed that those who use nicotine spent more time in the FI-DMN, having greater trauma-related emotional dysregulation is linked with less time in this same network. Thus, considering trauma-related factors revealed an alternative neurobiological underpinning of nicotine use which was not seen when only comparing those who do and do not smoke. Our findings also suggests that too much or too little FI-DMN function may correspond with different aspects of emotional dysregulation (i.e., too much or too little focus on emotional states), which both contribute to nicotine use.

Publication Information

Quam, Annika; Biernacki, Kathryn; Ross, Thomas J; Salmeron, Betty Jo; Janes, Amy C

Childhood Trauma, Emotional Awareness, and Neural Correlates of Long-Term Nicotine Smoking Journal Article

In: JAMA Netw Open, vol. 7, no. 1, pp. e2351132, 2024, ISSN: 2574-3805.

Abstract | Links

@article{pmid38206627,
title = {Childhood Trauma, Emotional Awareness, and Neural Correlates of Long-Term Nicotine Smoking},
author = {Annika Quam and Kathryn Biernacki and Thomas J Ross and Betty Jo Salmeron and Amy C Janes},
url = {https://pubmed.ncbi.nlm.nih.gov/38206627/},
doi = {10.1001/jamanetworkopen.2023.51132},
issn = {2574-3805},
year = {2024},
date = {2024-01-01},
urldate = {2024-01-01},
journal = {JAMA Netw Open},
volume = {7},
number = {1},
pages = {e2351132},
abstract = {IMPORTANCE: Temporal dynamic measures provide insight into the neurobiological properties of nicotine use. It is critical to determine whether brain-based measures are associated with substance use risk factors, such as childhood trauma-related emotion dysregulation.nnOBJECTIVE: To assess temporal dynamic differences based on smoking status and examine the associations between childhood trauma, alexithymia, nicotine smoking, and default mode network (DMN) states.nnDESIGN, SETTING, AND PARTICIPANTS: This cross-sectional study was conducted in the Baltimore, Maryland, area at the National Institute on Drug Abuse. Participants included individuals aged 18 to 65 years who smoked nicotine long term and matched controls with no co-occurring substance use or psychiatric disorders. Participants were enrolled from August 8, 2013, to August 9, 2022. Analysis was conducted from August 2022 to July 2023.nnEXPOSURE: Long-term nicotine smoking.nnMAIN OUTCOMES AND MEASURES: The main outcome was temporal dynamic differences based on smoking status. Coactivation pattern analysis was conducted based on 16-minute resting-state functional magnetic resonance imaging; total time in, persistence of, and frequency of transitions into states were evaluated. The associations between childhood trauma (Childhood Trauma Questionnaire), alexithymia (20-item Toronto Alexithymia Scale), and DMN temporal dynamics were assessed.nnRESULTS: The sample included 204 participants (102 individuals who smoked nicotine and 102 control individuals) with a mean (SD) age of 37.53 (10.64) years (109 [53.4%] male). Compared with controls, individuals who smoked nicotine spent more time in the frontoinsular DMN (FI-DMN) state (mean difference, 25.63 seconds; 95% CI, 8.05-43.20 seconds; η2p = 0.04; P = .004 after Bonferroni correction). In those who smoked nicotine, greater alexithymia was associated with less time spent in the FI-DMN state (r, -0.26; 95% CI, -0.44 to -0.07; P = .007). In a moderated mediation analysis, alexithymia mediated the association between childhood trauma and time spent in the FI-DMN state only in individuals who smoked nicotine (c' = -0.24; 95% CI, -0.58 to -0.03; P = .02).nnCONCLUSIONS AND RELEVANCE: Compared with controls, individuals who smoked nicotine spent more time in the FI-DMN state. Among those who smoked nicotine, childhood trauma-related alexithymia was associated with less time spent in the FI-DMN state, indicating that considering trauma-related factors may reveal alternative neurobiological underpinnings of substance use. These data may aid in reconciling contradictory findings in prior literature regarding the role of FI-DMN regions in substance use.},
keywords = {},
pubstate = {published},
tppubtype = {article}
}

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IMPORTANCE: Temporal dynamic measures provide insight into the neurobiological properties of nicotine use. It is critical to determine whether brain-based measures are associated with substance use risk factors, such as childhood trauma-related emotion dysregulation.nnOBJECTIVE: To assess temporal dynamic differences based on smoking status and examine the associations between childhood trauma, alexithymia, nicotine smoking, and default mode network (DMN) states.nnDESIGN, SETTING, AND PARTICIPANTS: This cross-sectional study was conducted in the Baltimore, Maryland, area at the National Institute on Drug Abuse. Participants included individuals aged 18 to 65 years who smoked nicotine long term and matched controls with no co-occurring substance use or psychiatric disorders. Participants were enrolled from August 8, 2013, to August 9, 2022. Analysis was conducted from August 2022 to July 2023.nnEXPOSURE: Long-term nicotine smoking.nnMAIN OUTCOMES AND MEASURES: The main outcome was temporal dynamic differences based on smoking status. Coactivation pattern analysis was conducted based on 16-minute resting-state functional magnetic resonance imaging; total time in, persistence of, and frequency of transitions into states were evaluated. The associations between childhood trauma (Childhood Trauma Questionnaire), alexithymia (20-item Toronto Alexithymia Scale), and DMN temporal dynamics were assessed.nnRESULTS: The sample included 204 participants (102 individuals who smoked nicotine and 102 control individuals) with a mean (SD) age of 37.53 (10.64) years (109 [53.4%] male). Compared with controls, individuals who smoked nicotine spent more time in the frontoinsular DMN (FI-DMN) state (mean difference, 25.63 seconds; 95% CI, 8.05-43.20 seconds; η2p = 0.04; P = .004 after Bonferroni correction). In those who smoked nicotine, greater alexithymia was associated with less time spent in the FI-DMN state (r, -0.26; 95% CI, -0.44 to -0.07; P = .007). In a moderated mediation analysis, alexithymia mediated the association between childhood trauma and time spent in the FI-DMN state only in individuals who smoked nicotine (c' = -0.24; 95% CI, -0.58 to -0.03; P = .02).nnCONCLUSIONS AND RELEVANCE: Compared with controls, individuals who smoked nicotine spent more time in the FI-DMN state. Among those who smoked nicotine, childhood trauma-related alexithymia was associated with less time spent in the FI-DMN state, indicating that considering trauma-related factors may reveal alternative neurobiological underpinnings of substance use. These data may aid in reconciling contradictory findings in prior literature regarding the role of FI-DMN regions in substance use.

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  • https://pubmed.ncbi.nlm.nih.gov/38206627/
  • doi:10.1001/jamanetworkopen.2023.51132

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