Sleep Deprivation Is Associated with Attenuated Parametric Valuation and Control Signals in the Midbrain during Value-Based Decision Making

Abstract

Sleep deprivation (SD) has detrimental effects on cognition, but the affected psychological processes and underlying neural mechanisms are still essentially unclear. Here we combined functional magnetic resonance imaging and computational modeling to examine how SD alters neural representation of specific choice variables (subjective value and decision conflict) during reward-related decision making. Twenty-two human subjects underwent two functional neuroimaging sessions in counterbalanced order, once during rested wakefulness and once after 24 h of SD. Behaviorally, SD attenuated conflict-dependent slowing of response times, which was reflected in an attenuated conflict-induced decrease in drift rates in the drift diffusion model. Furthermore, SD increased overall choice stochasticity during risky choice. Model-based functional neuroimaging revealed attenuated parametric subjective value signals in the midbrain, parietal cortex, and ventromedial prefrontal cortex after SD. Conflict-related midbrain signals showed a similar downregulation. Findings are discussed with respect to changes in dopaminergic signaling associated with the sleep-deprived state.

Sleep and impulsivity in Parkinson's disease

“…Sleep deprivation and sleepiness are known to increase impulsive behavior [11,12], either via disruption of the prefrontal cortex [13,14], which would otherwise provide top-down inhibitory control of impulsive behavior, or by amplifying the reactivity of brain reward networks [29]. Moreover, PD is associated with impairments to sleep including sleep fragmentation [30].…”

“…Sleep deprivation and fragmentation have been linked causally to a lack of control over impulsive behavior in healthy adults [11,12], presumably due to sleep-loss-related impairments in prefrontal cortex top-down inhibitory control [13,14]. Likewise, sleep fragmentation has been linked to impulsiveness in other clinical populations including attention-deficit/hyperactivity disorder (ADHD)[15] and restless legs syndrome (RLS)[16].…”

The sleep-deprived human brain

“…Equally important, not all human SD studies have reported amplified basal ganglia activity during reward-related decision making 49 , an inconsistency we return to below.…”

Sleep and dreaming are for important matters

“…In light of the recent findings on the consequences of total sleep deprivation and REM sleep deprivation on emotional and reward functions at the behavioral (Killgore et al, 2006; Banks and Dinges, 2007), neurobiological (Venkatraman et al, 2007; Yoo et al, 2007; Gujar et al, 2011b; Menz et al, 2012) and clinical (Riemann et al, 2002; Salvadore et al, 2010) levels, we propose here that REM sleep cannot be reduced to a depressiogenic sleep stage, but may instead have a crucial role in the maintenance of the integrity of emotional and reward networks. Indeed, perturbation of these networks with total or partial sleep deprivation leads to reduced disappointment in response to losses, together with decreased activity in the insular cortex (Venkatraman et al, 2007), which is thought to process the emotional significance of a stimulus, including the somatic affective response and awareness (Ernst and Paulus, 2005).…”

“…Indeed, perturbation of these networks with total or partial sleep deprivation leads to reduced disappointment in response to losses, together with decreased activity in the insular cortex (Venkatraman et al, 2007), which is thought to process the emotional significance of a stimulus, including the somatic affective response and awareness (Ernst and Paulus, 2005). Moreover, sleep deprivation caused attenuated conflict sensitivity for trials yielding high decision conflict (relatively large amounts associated with relatively low probability of winning) in a risky choice task, paralleled by a downregulation of conflict-related signals in the SN/VTA (Menz et al, 2012). A failure of top-down cortical control from the mPFC on the amygdala (Yoo et al, 2007), and an amplified reactivity of reward networks in response to positive emotional stimuli (Gujar et al, 2011b) have been also described as consequences of sleep deprivation.…”