Hyperactivation to pleasant interoceptive stimuli characterizes the transition to stimulant addiction

Abstract

Aims: Altered interoception, how the brain processes afferents from the body, may contribute to the urge to take drugs, and subsequently, the development of addiction. Although chronic stimulant dependent individuals exhibit attenuated brain responses to pleasant interoceptive stimuli, it is unclear whether this deficit exists early-on in the process of transition to stimulant addiction.

Methods: To this end, we compared problem stimulant users (PSU; n=18), desisted stimulant users (DSU; n=15), and stimulant naïve comparison subjects (CTL; n=15) during functional magnetic resonance imaging (fMRI) while they anticipated and experienced pleasant soft touch (slow brushstroke to the palm and forearm).

Results: Groups did not differ in behavioral performance or visual analog scale ratings of soft touch stimuli. fMRI results indicated that PSU exhibited greater right anterior insula, left inferior frontal gyrus, and right superior frontal gyrus activation than DSU and CTL during the anticipation and experience of soft touch. Moreover, during the experience of soft touch, PSU demonstrated higher bilateral precentral gyrus/middle insula and right posterior temporal gyrus activation than DSU and CTL.

Conclusions: In contrast to chronic stimulant dependence, individuals who have recently developed stimulant use disorders show exaggerated neural processing of pleasant interoceptive stimuli. Thus, increased processing of body-relevant information signaling pleasant touch in those individuals who develop problem use may be a predictive interoceptive biomarker. However, future investigations will need to determine whether the combination of probing pleasant interoception using neuroimaging is sufficiently sensitive and specific to help identify individuals at high risk for future problem use.

Keywords: Amphetamine; Cocaine; Functional magnetic resonance imaging; Interoception; Reward.

Figure 1

(A) Illustration of the Soft Touch paradigm, wherein participants anticipated or experienced a soft touch brushstroke on their forearm (signaled by yellow background) or palm (signaled by a blue background); (B) Illustration of normalized condition (anticipation, soft touch) and stimulus type (forearm, palm) regressors included in the fMRI deconvolution as a function of repetition time (TR) during one run of the task.

Figure 2

Neuroimaging results for: (A) the group main effect, wherein problem stimulant users (PSU) exhibited greater left inferior frontal gyrus (IFG), right anterior insula (AI), and right superior frontal gyrus (SFG) activation than desisted stimulant users (DSU) and healthy comparison subjects (CTL) across anticipation and soft touch trials. PSU also displayed greater activation than CTL in right IFG but did not differ from DSU according to Bonferroni corrections; and (B) the group x condition interaction, wherein PSU displayed higher bilateral precentral gyrus (PCG)/middle insula (MI) activation than DSU and CTL during the soft touch condition but not the anticipation condition. Error bars reflect + 1 standard error of the mean.