Sleep deprivation amplifies striatal activation to monetary reward

Abstract

Background: Sleep loss produces abnormal increases in reward seeking but the mechanisms underlying this phenomenon are poorly understood. The present study examined the influence of one night of sleep deprivation on neural responses to a monetary reward task in a sample of late adolescents/young adults.

Method: Using a within-subjects crossover design, 27 healthy, right-handed late adolescents/young adults (16 females, 11 males; mean age 23.1 years) underwent functional magnetic resonance imaging (fMRI) following a night of sleep deprivation and following a night of normal sleep. Participants’ recent sleep history was monitored using actigraphy for 1 week prior to each sleep condition.

Results: Following sleep deprivation, participants exhibited increased activity in the ventral striatum (VS) and reduced deactivation in the medial prefrontal cortex (mPFC) during the winning of monetary reward, relative to the same task following normal sleep conditions. Shorter total sleep time over the five nights before the sleep-deprived testing condition was associated with reduced deactivation in the mPFC during reward.

Conclusions: These findings support the hypothesis that sleep loss produces aberrant functioning in reward neural circuitry, increasing the salience of positively reinforcing stimuli. Aberrant reward functioning related to insufficient sleep may contribute to the development and maintenance of reward dysfunction-related disorders, such as compulsive gambling, eating, substance abuse and mood disorders.

Figure 1

A) Significantly greater activity to reward following sleep deprivation compared to the normal sleep condition in the left VS (t (25)=2.60, p=0.005, k=61 [peak voxel: x=−10, y=10, z=−8 in MNI space]). The bar graph represents mean blood-oxygen-level-dependent (BOLD) signal change in each sleep condition during reward and loss blocks relative to control blocks across all voxels within the cluster; the error bars represent standard error of the mean. B) Significantly greater activity to win-loss following sleep deprivation compared to the normal sleep condition in the left VS (t (25)=2.66, p=0.007, k=62 [peak voxel: x=−12, y=16, z=−4 in MNI space]). The bar graph represents mean BOLD signal change in each sleep condition during reward blocks relative to loss blocks across all voxels within the cluster; the error bars represent standard error of the mean. Within-group differences to reward across sleep conditions were significant using a voxelwise threshold of p<0.05 corrected for family wise error using AlphaSim Monte Carlo simulation.

Figure 2

A) Significantly increased activation of left mPFC to reward-control following sleep deprivation compared to the normal sleep condition (t (25)=2.92, p=0.002, k=184 [peak voxel: x=−14, y=42, z=4 in MNI space]). The bar graph represents mean BOLD signal change in each sleep condition during reward and loss blocks relative to control blocks across all voxels within the cluster; the error bars represent standard error of the mean. The loss bars are included for illustrative purposes, and are not significantly different between sleep conditions. Within-group differences to reward across sleep conditions were significant using a voxelwise threshold of p<0.05 corrected for family wise error using AlphaSim Monte Carlo simulation. B) Cluster within the mPFC region of interest mask showing a significant negative relationship with recent sleep history (i.e., actigraphy-derived mean total sleep time in five nights prior to the experimental night in the laboratory preceding the fMRI scan) during reward trials under the sleep deprived condition (bilateral rostral anterior cingulate cortex; t (21)=4.06, p<0.001, k=1436 [peak voxel: x=18, y=44, z=20 in MNI space]). The scatterplot represents mean total sleep time before the sleep deprivation condition plotted against mean BOLD signal change during reward relative to control blocks across all voxels in the highlighted cluster within the mPFC. Regression analyses were significant using a voxelwise threshold of p<0.05 corrected for family wise error using AlphaSim Monte Carlo simulation.