Electrophysiological signature of the interplay between habits and inhibition in response to smoking-related cues in individuals with a smoking habit: An event-related potential study

Abstract

The rigid, stimulus-bound nature of drug seeking that characterizes substance use disorder (SUD) has been related to a dysregulation of motivational and early attentional reflexive and inhibitory reflective systems. However, the mechanisms by which these systems are engaged by drug-paired conditioned stimuli (CSs) when they promote the enactment of seeking habits in individuals with a SUD have not been elucidated. The present study aimed behaviourally and electrophysiologically to characterize the nature of the interaction between the reflexive and reflective systems recruited by CSs in individuals with a smoking habit. We measured the behavioural performance and associated event-related potentials (ERPs) of 20 individuals with a smoking habit and 20 controls, who never smoked regularly, in a modified Go/NoGo task during which smoking-related CSs, appetitive and neutral pictures, presented either in first or third-person visual perspective were displayed 250 ms before the Go/NoGo cue. We show that smoking-related cues selectively influence early incentive motivation-related attention bias (N2 after picture onset), motor readiness and behavioural inhibition (Go-P3, NoGo-P3 and Pc) of individuals with a smoking habit only when presented from a first-person visual perspective. These data together identify the neural signature of the aberrant engagement of the reflexive and reflective systems during the recruitment of an incentive habit by CSs presented as if they had been response-produced, that is, as conditioned reinforcers.

Keywords: EEG ERP; cue reactivity; habits; inhibition; smoking habit.

FIGURE 1

Example of smoking‐related, appetitive or neutral pictures presented either from a first‐ or third‐person visual perspective.

FIGURE 2

The N200 reflects selective attention capture by drug‐paired cues in smokers. Top panel. ERPs, and especially the P100, evoked in Pz by pictures from a first‐ (light purple) vs. third‐person (dark purple) visual perspective (VP) (a) are represented alongside the P100 mean electrical voltage (μV) over the scalp (b) and its source estimation (LORETA) (c). The P100 evoked by 3‐VP pictures were more negative than those evoked by 1‐VP pictures. Bottom panel. ERPs, and especially the N200, evoked in Fz by neutral, appetitive and smoking‐related pictures in smokers and controls (d) are represented alongside the N200 mean electrical voltage (μV) in central electrodes (e1) (e) and its source estimation (LORETA) (f). Smokers evoked a less negative N200 than controls when presented with a smoking‐related picture. No differences were observed between smokers and controls in the N200 evoked by neutral and appetitive pictures. Note that source estimations of both P100 and N200 effects point to similar putative sources in cortical areas (BA 31 and 7, respectively). *p < .05.

FIGURE 3

A late P3 selectively tracks the smoking‐related cues presented from a first‐person visual perspective in smokers. (a) The late P3 (420–470 ms) evoked at the F4 electrode following Go or NoGo cues differed between smokers and controls when presented with smoking‐related 1‐VP pictures. The electrical map (b) and source estimation in smokers (c) and controls (d) suggested that the P3 may be associated with alterations in frontal modulations in both smokers and controls (BA 10 and 32). (e) Subsequent analysis of the residual ERP evoked by smoking‐related pictures in Go trials only revealed a differential impact of the visual perspective (the 1‐VP minus 3‐VP) in smokers as compared with controls. The electrical map (f) and the source estimation in smokers (g) and controls (h) suggested that this difference may potentially be due to alterations in modulations of Brodmann area (BA) 23 and 10 in smokers and controls, respectively. (i) In contrast, the residual ERP evoked by smoking‐related pictures presented in NoGo trials revealed a reverse visual perspective effect (1‐VP minus 3‐VP) in each group compared with Go trials. The electrical map (j) and the source estimation in smokers (k) and controls (l) suggested that the P3‐NoGo may present a frontal distribution (BA 10 and 11) in both smokers and controls. *p < .05.

FIGURE 4

The motor response‐locked Pc in Go trials is greater in smokers for smoking‐related pictures than for appetitive and neutral pictures. (a–c) The amplitude of the Pc (in Cz) evoked by smokers tracked only the difference between responses made with smoking‐related 1‐VP pictures and those made with appetitive and neutral pictures. The latter were associated with a response that evoked a similar Pc with a lower amplitude than that evoked by the former. Source estimation suggested that these effects may potentially be related to modulations of the frontal lobe (BA 6) (b and c). (d) The Pc evoked by smokers following a response made with smoking‐related 3‐VP pictures, which was of a greater amplitude than that evoked by the same pictures from a first‐person visual perspective (1‐VP), was also greater than that evoked by responses made with appetite and neutral pictures. However, when presented from a 3‐VP, appetitive pictures were associated with responses evoking greater Pc than neutral pictures. Source estimation suggested that these effects may be related to modulations of the orbitofrontal cortex (BA 10) (e and f). ^@ p < .05; *different from neural, p < 0.05; ^#different from appetitive, p < .05.