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. 2015 Dec;110(12):2025-36.
doi: 10.1111/add.13090. Epub 2015 Sep 28.

Under pressure: adolescent substance users show exaggerated neural processing of aversive interoceptive stimuli

Lotte Berk  1 , Jennifer L Stewart  2 , April C May  1 , Reinout W Wiers  3 , Paul W Davenport  4 , Martin P Paulus  1   5   6 , Susan F Tapert  1   6
Affiliations

Under pressure: adolescent substance users show exaggerated neural processing of aversive interoceptive stimuli

Lotte Berk et al. Addiction. 2015 Dec.

Abstract

Aims: Adolescents with substance use disorders (SUD) exhibit hyposensitivity to pleasant internally generated (interoceptive) stimuli and hypersensitivity to external rewarding stimuli. It is unclear whether similar patterns exist for aversive interoceptive stimuli. We compared activation in the insular cortex and other brain regions during the anticipation and experience of aversive stimuli between adolescents with SUD and those without.

Design: Cross-sectional experimental study with two groups.

Participants: Adolescents (ages 15-17 years) with an alcohol or marijuana SUD (n=18) and healthy comparison subjects (CON, n=15). Participants were recruited by distributing flyers at local high schools.

Setting: Keck Imaging Center, University of California San Diego, CA, USA.

Measurements: Behavioral and neural responses to a continuous performance task with inspiratory breathing load recorded during an fMRI session. Questionnaires assessed life-time drug use, anxiety, sensation-seeking, impulsivity, affect and bodily awareness. Visual analog scales assessed drug craving and breathing load responses.

Findings: Across subjects, experience of breathing load elicited greater bilateral anterior and posterior insula (AI and PI, respectively) activation than anticipation (F(1,31)=4.16, P<0.05). SUD exhibited greater left AI and bilateral PI activation during breathing load than anticipation, compared with CON (F(1,31)=4.16, P<0.05). In contrast, CON showed greater activation during anticipation than breathing load in left PI, compared with SUD (F(1,31)=4.16, P<0.05).

Conclusions: Adolescents with alcohol and marijuana substance use disorders may be hypersensitive to aversive interoceptive stimuli.

Keywords: Adolescence; alcohol; breathing load; cannabis; fMRI; interoception.

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Conflict of interest statement

All authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Inspiratory breathing load.
Figure 2
Figure 2
The main task effect showed greater bilateral insula activation during breathing load than anticipation across participants (F(1,31)=4.16, p<.05). Error bars reflect ± 1 standard error.
Figure 3
Figure 3
The group by condition interaction showed: (1) between-group differences, wherein adolescents with substance use disorder (SUD) exhibited greater right posterior insula and left anterior insula activation than healthy controls (CON) during breathing load; and (2) within-group differences, wherein SUD exhibited consistent modulation in bilateral posterior insula and left anterior insula as a function of anticipation and breathing load conditions, but CON did not. Error bars reflect ± 1 standard error. * p=<.05; **p<.01.
Figure 4
Figure 4
The group by condition interaction showed: (1) between-group differences, wherein adolescents with substance use disorder (SUD) exhibited greater left middle frontal gyrus and right inferior frontal gyrus than healthy controls (CON) during breathing load; and (2) within-group differences, wherein SUD exhibited consistent modulation in these regions as a function of anticipation and breathing load conditions, but CON did not. Error bars reflect ± 1 standard error. * p=<.05; **p<.01.
Figure 5
Figure 5
Brain activation during breathing load in adolescents with substance use disorder (SUD). SUD exhibited a negative relationship between (a) left middle frontal gyrus (r=−.62, p=.02) and (b) right posterior insula (r=−.58, p=.02) and Body Awareness Questionnaire (BAQ) scores. Brain activation during breathing load for SUD shows a positive relationship between (c) left middle frontal gyrus and visual analogue scale (VAS) intensity of the breathing load (r=.52, p=.05). SUD exhibited a negative relationship between (d) right inferior frontal gyrus and sensation seeking (SSS; r=−.56, p=.04).
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