Front. Behav. Neurosci. | doi: 10.3389/fnbeh.2016.00154
Paula Banca1*, Valerie Voon2, 3 and Neil A. Harrison4
- 1Behavioural and Clinical Neuroscience Institute, University of Cambridge, United Kingdom
- 2Department of Psychiatry, University of Cambridge, United Kingdom
- 3Cambridgeshire and Peterborough NHS Foundation Trust, United Kingdom
- 4Brighton and Sussex Medical School, University of Sussex, United Kingdom
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 use disorder (AUD) 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 AUD and pathological video-gaming were slower at reversal learning irrespective of valence, with AUD 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 AUD relative to healthy volunteers. This study provides evidence for commonalities and differences in two distinct dimensions of behavioral inflexibility across disorders of compulsivity. 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 AUD 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.
Keywords: Addiction, alcohol dependence, Binge Eating Disorder, compulsivity, Reversal Learning, Set-shifting.
Citation: Banca P, Voon V and Harrison NA (2016). Compulsivity across the pathological misuse of drug and non-drug rewards. Front. Behav. Neurosci. 10:154. doi: 10.3389/fnbeh.2016.00154
Received: 14 Apr 2016; Accepted: 19 Jul 2016.
Edited by: Matthias Brand, University of Duisburg, Germany
Reviewed by:
Alicia Izquierdo, University of California, Los Angeles, USA
Juan M. Dominguez, University of Texas at Austin, USA
Rudolf Stark, University of Giessen, Germany
* Correspondence: Dr. Paula Banca, University of Cambridge, Behavioural and Clinical Neuroscience Institute, Cambridge, United Kingdom, [email protected]
ABSTRACT
CSB subjects demonstrated enhanced sensitivity to reward outcomes with faster acquisition and greater perseveration with higher magnitude rewards
RESULTS
Trails to criterion: In the Reversal phase in the CSB subjects (N=25) compared to healthy volunteers (N=50) there was no main effect of Group (F(1,73)=1.33, p=0.253), Valence (F(1,73)=1.47, p=0.229) or interaction effect (F(1,73)=0.008, p=0.928) (Figure 1). In the Acquisition phase in the CSB subjects (Reward: HV 9.39 (SD 7.34); CSB 6.39 (SD 5.43); Loss: HV 7.26 (SD 6.53); CSB 8.69 (SD 7.83)) there was a Group x Valence interaction (F(1,73)=4.35, p=0.039) in which CSB subjects were faster to learn from Rewards and slower to learn from Losses as compared to healthy volunteers. There was no Group (F(1,73)=0.38, p=0.539) or Valence effect (F(1,73)<0.001, p=0.983 Win-Stay/Lose-Shift: In the Lose-Shift analysis, there was a Group x Valence effect (Table 3; Figure 2); in the posthoc analysis, CSB subjects had lower Lose-Shift or were more likely to stay or perseverate after a loss in the Reward condition relative 422 to Loss (p=0.005) and Neutral (p<0.001). Similarly, in the Win-Stay analysis, there was a Group x Valence effect; in the posthoc analysis, CSB had higher Win-Stay or were more likely to stay after a win in the Reward condition relative to Loss (p=0.019) and Neutral (p=0.007). 427
Summary: CSB subjects were faster to learning from rewards in the acquisition phase compared to healthy volunteers and were more likely to perseverate or stay after either a loss or a win in the Reward condition.
DISCUSSION
The literature consistently implicates differing aspects of fronto-striatal circuitry in reversal learning and attentional set-shifting, namely orbitofrontal and lateral prefrontalcortices respectively. We have previously reported on these measures of reversal learning (number of trials to criterion) and ED shifting demonstrating a relationship between dissociable fronto-striatal circuits (Morris et al., 2016).
In contrast to other disorders, CSB compared to healthy volunteers showed faster acquisition to reward outcomes along with a greater perseveration in the reward condition irrespective of outcome. The CSB subjects did not show any specific impairments in set shifting or reversal learning. These findings converge with our previous findings of enhanced preference for stimuli conditioned to either sexual or monetary outcomes, overall suggesting enhanced sensitivity to rewards (Banca et al., 2016). Further studies using salient rewards are indicated. Deficits in goal-directed or exploratory behaviors in CSB have not yet been reported.
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