Abstract
Behavioral adaptation is required for the successful navigation of a constantly changing environment. Impairments in behavioral flexibility are commonly observed in psychiatric disorders including those of addiction. This study investigates two distinct facets of compulsivity, namely reversal learning and attentional set shifting, implicating orbitofrontal and lateral prefrontal regions respectively, across disorders of primary and secondary rewards. Obese subjects with and without binge eating disorder (BED), individuals with compulsive sexual behaviors (CSB), alcohol dependence (AD) and pathological video-gaming (VG) were tested with two computerized tasks: the probabilistic reversal task (trials to criterion and win-stay/lose-shift errors) and the intra/extra-dimensional set shift task (IED). Individuals with AD and pathological VG were slower at reversal learning irrespective of valence, with AD subjects more likely to perseverate after losses. Compared to obese subjects without BED, BED subjects were worse at reversal learning to wins but better at losses highlighting valence effects as a function of binge eating. CSB subjects demonstrated enhanced sensitivity to reward outcomes with faster acquisition and greater perseveration with higher magnitude rewards. We further show an impairment in attentional set shifting in individuals with BED and AD relative to healthy volunteers (HV). This study provides evidence for commonalities and differences in two distinct dimensions of behavioral inflexibility across disorders of compulsivity. We summarize studies on compulsivity subtypes within this same patient population. We emphasize commonalities in AD and BED with impairments across a range of compulsivity indices, perhaps supporting pathological binge eating as a form of behavioral addiction. We further emphasize commonalities in reversal learning across disorders and the crucial role of valence effects. These findings highlight the role of behavioral inflexibility and compulsivity as a relevant domain in defining dimensional psychiatry and the identification of relevant cognitive endophenotypes as targets for therapeutic modulation.
Highlights
The ability to adjust behaviors is crucial for optimal navigation in a constantly changing environment
Obese Subjects With and Without binge eating disorder (BED) Trials to criterion In the Reversal phase (Figure 1) in BED (N = 32) subjects compared to healthy volunteers (HV) (N = 64) there was no main effect of Valence (F(1,94) = 0.12, p = 0.726), or Group (F(1,94) = 1.19, p = 0.278) or Group × Valence interaction (F(1,94) = 3.04, p = 0.085)
Alcohol Dependence Trials to criterion In the Reversal phase in the alcohol dependence (AD) subjects (N = 32) vs. HV (N = 64) there was a main effect of Group F(1,94) = 5.78, p = 0.018) in which AD subjects required more trials to reach criterion compared to HV (Figure 1)
Summary
The ability to adjust behaviors is crucial for optimal navigation in a constantly changing environment. Reversal learning measures the capacity to flexibly switch choices with changes in contingencies and implicates orbitofrontal cortices whereas attentional set shifting is the ability to shift response sets to a previously irrelevant dimension and implicates lateral prefrontal cortices (Kringelbach and Rolls, 2003; McAlonan and Brown, 2003; O’Doherty et al, 2003; Hornak et al, 2004; Robbins, 2007) Deficits in these markers of cognitive inflexibility have been classically studied across species (for review on reversal learning see Izquierdo et al, 2016; and on attentional set shifting see Brown and Tait, 2016; Izquierdo et al, 2016). In keeping with the trend towards dimensional psychiatry (Insel et al, 2010), we seek to compare the cross-diagnostic neurocognitive profile focusing on compulsivity to enhance our understanding of current psychiatric disorder classifications (Robbins et al, 2012)
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