Elsevier

Drug and Alcohol Dependence

Volume 159, 1 February 2016, Pages 277-280
Drug and Alcohol Dependence

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Insula reactivity to negative stimuli is associated with daily cigarette use: A preliminary investigation using the Human Connectome Database

https://doi.org/10.1016/j.drugalcdep.2015.12.010Get rights and content

Highlights

  • Prior work shows the insula’s role in nicotine dependence and affective processing.

  • We evaluated the link between insula reactivity to negative affect and cigarette use.

  • Smokers using more cigarettes/day have greater insula reactivity to negative stimuli.

  • Individual variability in affective processing is associated with cigarette use.

Abstract

Background

Individuals who smoke more cigarettes per day are at greater risk for developing smoking-related illness and have more difficulty quitting. Withdrawal-related negative mood is one factor thought to motivate drug use. However, heavy smokers are generally more sensitive to negative affect, not just negative emotion stemming from withdrawal. One possibility is that individual differences in how the brain processes negative stimuli may impact smoking use. Given the wealth of data implicating the insula in nicotine dependence and affective processing we hypothesize that the number of cigarettes an individual smokes per day will relate to insula reactivity to negative stimuli.

Methods

A functional magnetic resonance imaging (fMRI) emotional processing task collected by the Human Connectome Project was assessed in 21 daily tobacco smokers who reported smoking between 5 and 20 cigarettes per day. The number of cigarettes smoked per day was correlated with right and left anterior insula reactivity to faces expressing a negative emotion relative to a control. This anterior insula region of interest has been associated with treatment outcome and smoking cue-reactivity in our prior work.

Results

Those who smoked more daily cigarettes showed greater right insula reactivity to negative stimuli (r = 0.564, p = 0.008). Left insula reactivity was not associated with cigarettes smoked per day.

Conclusion

Smokers who use more cigarettes per day have greater insula reactivity to negative stimuli, furthering the field's understanding of the insula's involvement in nicotine use. This preliminary work also suggests a mechanism contributing to higher rates of daily smoking.

Introduction

Over 36 million adults in the United States smoke cigarettes daily (Centers for Disease Control and Prevention (CDC), 2010), yet the number of cigarettes smoked/day varies across individuals (Shiffman, 2009, Burns et al., 1997). Understanding factors influencing smoking rates is essential, as greater smoking rates are associated with increased risk of smoking related illness (Bjartveit and Tverdal, 2005, Law and Wald, 2003) and with poorer quit outcomes (Harris et al., 2004, Hymowitz et al., 1997).

One factor possibly mediating daily cigarette use is reactivity to negative affect, as smoking is often maintained to alleviate negative mood states (Copeland et al., 1995, Brandon, 1994, Baker et al., 2004). Smokers self-administer greater numbers of cigarettes/day when faced with exogenous stressors (Aronson et al., 2008) and more rapid relapse is associated with decreased distress tolerance (Brown et al., 2002), suggesting that smoking may be related to how an individual processes negative affect. To test the hypothesis that daily smoking rates are associated with how negative affect is processed, we evaluated the relationship between the number of cigarettes an individual smokes/day and insula reactivity to negative stimuli.

Insula reactivity to negative stimuli in smokers is of particular interest, because this brain region is implicated in affective processing (Critchley, 2002, Critchley et al., 2004, Damasio et al., 2000, Phan et al., 2002, Craig, 2002, Craig, 2010) and smoking (Janes et al., 2010a, Janes et al., 2010b, Naqvi et al., 2007, Gray and Critchley, 2007). The insula is engaged during the processing of basic affective states, including the interpretation of external stimuli such as emotional faces (Carr et al., 2003) and internal awareness of one’s emotions (Critchley, 2002, Critchley et al., 2004, Damasio et al., 2000, Craig, 2002, Craig, 2010). Additionally, the insula facilitates nicotine seeking-behavior (Naqvi et al., 2007, Forget et al., 2010, Scott and Hiroi, 2011, Pushparaj et al., 2013) and is related to factors that impact daily smoking such as cigarette craving (Brody et al., 2002, Wang et al., 2007) and nicotine dependence severity (Claus et al., 2013). Thus, our analysis focused on a previously identified anterior insula region of interest (ROI) that is associated with smoking (Janes et al., 2015).

To identify an association between daily cigarette use and insula reactivity to negative stimuli, we investigated data collected via the Human Connectome Project (HCP; Van Essen et al., 2013). Specifically, we assessed whether the number of cigarettes smoked/day was correlated with insula activity collected during an emotional processing task where individuals were presented with faces expressing negative emotion compared to a neutral control. Given the insula's involvement in both emotional processing and nicotine dependence, we hypothesize that insula reactivity to negative stimuli will be associated with greater daily nicotine use.

Section snippets

Participants

Data analyzed were obtained from the Human Connectome Project (HCP). A description of the recruitment criteria for the HCP is provided by Van Essen et al. (2013). Briefly, individuals were excluded by the HCP if they reported a significant history of psychiatric disorder, substance abuse, neurological disorder, or medical disorder known to influence brain function. Participants in the current study included all those reporting regular cigarette use who did not have a positive urine sample

Association between Insula reactivity and cigarettes/day

There was a positive association between cigarettes smoked/day and reactivity to negative faces > shapes in the right (Pearson’s r = 0.564, p = 0.008; Fig. 1), but not left anterior insula (Pearson’s r = 0.253, p = 0.268). This finding was supported by non-parametric testing using Spearman’s rho (right anterior insula r = 0.653, p = 0.001). While there was a marginal association between cigarettes smoked/day and beta weights extracted from the right posterior insula (Pearson’s r = 0.446, p = 0.43), this

Discussion

Negative affect is associated with nicotine use (Kassel et al., 2003, Hughes et al., 1994), as ameliorating withdrawal-related negative affect is one of the most cited reasons for precipitating relapse (Copeland et al., 1995, Brandon, 1994, Baker et al., 2004). The current finding expands our understanding of the link between negative affect and daily cigarette use by demonstrating that right anterior insula reactivity to negative stimuli is positively correlated with cigarettes smoked/day.

Role of funding

This study was supported by NIH funded grants: K01 DA029645 (PI Amy Janes) and T32 DA015036 (Supported author ND; PI Scott Lukas). Data were provided by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University.

Contributors

AJ defined the question and guided data analysis and manuscript preparation, ND and AP contributed to data analysis and wrote the manuscript. All authors approved the final version of the manuscript.

Conflict of interest

No conflict declared for any author.

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    Authors contributed equally to this work.

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