Is decreased prefrontal cortical sensitivity to monetary reward associated with impaired motivation and self-control in cocaine addiction?

Abstract

Objective: This study attempted to examine the brain's sensitivity to monetary rewards of different magnitudes in cocaine abusers and to study its association with motivation and self-control.

Method: Sixteen cocaine abusers and 13 matched healthy comparison subjects performed a forced-choice task under three monetary value conditions while brain activation was measured with functional magnetic resonance imaging. Objective measures of state motivation were assessed by reaction time and accuracy, and subjective measures were assessed by self-reports of task engagement. Measures of trait motivation and self-control were assessed with the Multidimensional Personality Questionnaire.

Results: The cocaine abusers demonstrated an overall reduced regional brain responsivity to differences between the monetary value conditions. Also, in comparison subjects but not in cocaine abusers, reward-induced improvements in performance were associated with self-reports of task engagement, and money-induced activations in the lateral prefrontal cortex were associated with parallel activations in the orbitofrontal cortex. For cocaine abusers, prefrontal cortex sensitivity to money was instead associated with motivation and self-control.

Conclusions: These findings suggest that in cocaine addiction 1) activation of the corticolimbic reward circuit to gradations of money is altered; 2) the lack of a correlation between objective and subjective measures of state motivation may be indicative of disrupted perception of motivational drive, which could contribute to impairments in self-control; and 3) the lateral prefrontal cortex modulates trait motivation and deficits in self-control, and a possible underlying mechanism may encompass a breakdown in prefrontal-orbitofrontal cortical communication.

Figure 1

SPM results of the monetary reward effect (45¢ or 1¢ > 0¢) in all subjects (A: comparison subjects, N=13, and cocaine abusers, N=16) and in direct group comparisons (B: comparison subjects > cocaine abusers). Statistical thresholds were p<0.005 uncorrected for A and p<0.05 uncorrected for B (third order analyses and a priori hypothesis), minimum cluster size was 5 contiguous voxels (135 mm³). CBL is cerebellum, OFC is orbitofrontal cortex, MSN is mesencephalon, OCC is occipital cortex, TH is thalamus, and PFC is prefrontal cortex.

Figure 2

Average BOLD signals in the ROIs (see Figure 1A and Table 1, regions in boldface) located at the left orbitofrontal cortex (A: OFC), prefrontal cortex (B: PFC, mean signal), right mesencephalon (C: MSN), and left cerebellum (D: CBL) as a function of monetary reward (white = 0¢; gray = 1¢; black = 45¢) and diagnostic group (left: 16 cocaine abusers; right: 12 comparison subjects, ss). Bar graphs represent mean % signal change from baseline ± SEM. ANOVA F results are presented on the right: df = 2, 25 (Money) or 1, 26 (Group). Results of significant t-tests are marked inside the figures: df = 11 (comparison subjects), 15 (cocaine), 26 (group differences); all significant t > |2.1|; *p<0.05; **p<0.01.

Figure 3

A: Correlation between the lateral PFC and inhibitory control in 16 cocaine abusers. Scatterplot shows association between the BOLD signal change for monetary reward as compared to the neutral cue (45¢ > 0¢) in the lateral PFC (x=33, y=36, z=15) with MPQ self-control (r=0.88, p = 0.001); the inserted statistical map of brain activation depicts the cluster location corresponding to this correlation (Table 2sC). Thresholded at p < 0.05 uncorrected. B: Correlation between the lateral PFC and OFC in 12 comparison subjects. Scatterplot shows association between the BOLD signal change for monetary reward as compared to baseline (45¢ > baseline) in the lateral PFC (x=−21, y=48, z=36) with same responses in the OFC (x=42, y=33, z=−12) (r=0.84, p = 0.001); the inserted statistical map of brain activation depicts the cluster location corresponding to this correlation (Table 2sD). Thresholded at p < 0.005 uncorrected. Minimum cluster size 100 contiguous voxels, 2700 mm³, for both.