Reward-Related Responses and Tonic Craving in Cocaine Addiction: An Imaging Study of the Monetary Incentive Delay Task - PubMed (original) (raw)
Reward-Related Responses and Tonic Craving in Cocaine Addiction: An Imaging Study of the Monetary Incentive Delay Task
Simon Zhornitsky et al. Int J Neuropsychopharmacol. 2021.
Abstract
Background: Cocaine addiction is associated with altered sensitivity to natural reinforcers and intense drug craving. However, previous findings on reward-related responses were mixed, and few studies have examined whether reward responses relate to tonic cocaine craving.
Methods: We combined functional magnetic resonance imaging and a monetary incentive delay task to investigate these issues. Imaging data were processed with published routines, and the results were evaluated with a corrected threshold. We compared reward responses of 50 cocaine-dependent individuals (CDs) and 45 healthy controls (HCs) for the ventral striatum (VS) and the whole brain. We also examined the regional responses in association with tonic cocaine craving, as assessed by the Cocaine Craving Questionnaire (CCQ) in CDs. We performed mediation analyses to evaluate the relationship between regional responses, CCQ score, and recent cocaine use.
Results: The VS showed higher activation to large as compared with small or no wins, but this reward-related activity did not differ between CDs and HCs. The precentral gyrus (PCG), anterior insula, and supplementary motor area showed higher activation during large vs no wins in positive correlation with the CCQ score in CDs. Mediation analyses suggested that days of cocaine use in the prior month contributed to higher CCQ scores and, in turn, PCG reward responses.
Conclusions: The results highlight a unique relationship between reward responses of the primary motor cortex, tonic cocaine craving, and recent cocaine use. The motor cortex may partake in the cognitive motor processes critical to drug-seeking behavior in addicted individuals.
Keywords: MIDT; cocaine dependence; fMRI; motor cortex; ventral striatum.
© The Author(s) 2021. Published by Oxford University Press on behalf of CINP.
Figures
Figure 1.
Behavioral paradigm and performance. (A) Monetary incentive delay task: a reward cue (a dollar, a cent, or no money) appeared at the beginning of each trial. After a randomized interval between 1 and 5 seconds, a target box appeared on the screen and disappeared after a short period (response window). Participants were told to press the button as quickly as possible to collect the money in the target box (win) before it disappeared. Otherwise, participants would lose the reward, with the amount deducted from the total win. A premature button-press prior to the appearance of the target box terminated the trial and similarly resulted in loss. A feedback window was shown on the screen after each trial to indicate the amount of money won or lost. (B) Accuracy rate and (C) Reaction time (RT) of dollar, cent and no money (nil) trials (mean ± SE). *P < .05.
Figure 2.
Regional activations to outcomes of (A) dollar win vs nil, (B) cent win vs nil, (C) dollar win vs cent win, (D) dollar loss vs nil, (E) cent loss vs nil, (F) dollar loss vs cent loss, (G) dollar win vs dollar loss, and (H) cent win vs cent loss in correlation with Cocaine Craving Questionnaire (CCQ) at voxel P < .001. Clusters meeting cluster-level P < .05 whole-brain corrected for familywise error of multiple comparisons are highlighted by insets and summarized in Table 2.
Figure 3.
Mediation analysis of Cocaine Craving Questionnaire (CCQ) score, days of cocaine use, and precentral gyrus activation of dollar win > nil. The P values associated with mediation are for the path a × b (see Methods). Only model E was significant at a corrected threshold P = .05/6 = .0083. The model suggested that tonic cocaine craving mediated the relationship between days of cocaine use and precentral gyrus activation during dollar wins > nil. The variables as descripted in Methods and included in (A) as an example applied to (B-F), too.
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References
- APA (2005) Diagnostic and statistical manual of mental disorders-IV-TR. Washington DC: American Psychiatric Association.
- Boutros NN, Lisanby SH, Tokuno H, Torello MW, Campbell D, Berman R, Malison R, Krystal JH, Kosten T (2001) Elevated motor threshold in drug-free, cocaine-dependent patients assessed with transcranial magnetic stimulation. Biol Psychiatry 49:369–373. - PubMed
- Bustamante JC, Barrós-Loscertales A, Costumero V, Fuentes-Claramonte P, Rosell-Negre P, Ventura-Campos N, Llopis JJ, Ávila C (2014) Abstinence duration modulates striatal functioning during monetary reward processing in cocaine patients. Addict Biol 19:885–894. - PubMed
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