The Neural Mechanisms of Social Reward in Early Psychosis

Anne-Kathrin J. Fett; Elias Mouchlianitis; Paula M. Gromann; Lucy Vanes; Sukhi S. Shergil; Lydia Krabbendam

Disclosures

Soc Cogn Affect Neurosci. 2019;14(8):861-870. 

In This Article

Abstract and Introduction

Abstract

In chronic psychosis, reduced trust is associated with a neural insensitivity to social reward and reduced theory of mind (ToM). Here we investigate whether these mechanisms could underlie emerging social impairments in early psychosis. Twenty-two participants with early psychosis and 25 controls (male, 13–19 years) participated in two interactive trust games against a cooperative and unfair partner. Region of interest neuroimaging analyses included right caudate, medial prefrontal cortex (mPFC) and right temporoparietal junction (rTPJ), involved in reward and ToM processing. Both groups showed similar levels of trust (i.e. investments). However, individuals with psychosis failed to activate the caudate differentially in response to cooperation and unfairness while making decisions to trust. During cooperative returns, patients showed reduced and controls increased caudate activation. Patients demonstrated greater rTPJ activation than controls, possibly pointing towards compensatory mechanisms. Effects were associated with Wechsler Abbreviated Scale of Intelligence vocabulary scores. No group differences emerged in mPFC activation. Early psychosis is associated with an aberrant neural sensitivity to social reward. This could foster reduced social motivation and social isolation. Absent behavioural differences in early, relative to chronic psychosis could indicate that trust is achieved through increased compensatory demand on ToM.

Introduction

The rewarding nature of social contact drives human social behaviour (Krach et al., 2010). The sensitivity to others' social signals is fundamental in understanding their behaviour in social interactions. Theory of mind (ToM), i.e. the ability to take another person's perspective into account, and social reward sensitivity, i.e. the ability to process positive or negative behavioural cues from others, enable us to build a mental model of them during our social encounters. Both social cognitive processes are therefore fundamental in social relationships, and impairment can lead to problematic social interactions.

Deficits in ToM and aberrant dopamine function (Kapur et al., 2005), which is closely linked to reward processing, have been suggested to underlie paranoia and social disconnection in psychosis (Kapur et al., 2005; Eisenberger & Cole, 2012). Supporting evidence for a direct association between aberrant social decision making and reward processing mechanisms comes from research with the interactive trust game (Berg et al., 1995). In this paradigm, the first player (investor) receives an endowment that he can share with the second player (trustee). The amount is tripled, and the trustee then decides whether to return a share of this overall amount or not. Cooperation yields the best payoff for both players, but initially the best payoff for the trustee occurs through not cooperating. For successful social interactions, it is crucial that intentions and goals of others are represented to optimise the mutual interaction (Yoshida et al., 2008). Theory of mind is necessary to anticipate the effects of one's own trusting decisions and to decipher the trustee's response, and better ToM abilities have been associated with a superior ability to adapt one's own decisions to the decision-making strategy of the trustee (Fett et al., 2014b). The ability to learn from the trustee's response through social reward or punishment is vital to establish whether trust pays off.

In the trust game, individuals with chronic nonaffective psychosis exhibit lower trust towards others than controls. Lower trust is associated with paranoid delusions, and the evidence suggests that low trust is maintained by reduced sensitivity to positive social information and reduced sensitivity to the game partner's actual trustworthy behaviour. In support of dysfunctional social reward and ToM processing as underlying mechanisms of reduced trust, neuroimaging research has associated the loss of trust with reduced activation of the right caudate nucleus, a key area of reward processing (King-Casas et al., 2005; Phan et al., 2010; Fett et al., 2012; Bhanji & Delgado, 2014) and the right temporoparietal junction (rTPJ), which underlies ToM (Gromann et al., 2013). Yet, the authors also reported normal activation patterns in the medial prefrontal cortex (mPFC), another area that has been related to ToM (Sanfey, 2007; Fett et al., 2015; Krueger & Meyer-Lindenberg, 2018; Porcelli et al., 2018). The aberrant neural mechanisms might lead to social impairment; however, they could also be secondary to exposure to other social or environmental factors that are associated with chronicity of illness. Typically, social impairments seem to emerge early in psychotic disorders, and adolescence is a crucial period for these changes (Velthorst et al., 2016). Social cooperation and ToM continue to develop during this stage (Blakemore, 2008; Fett et al., 2014a), emphasising its importance as a sensitive period for interventions that aim to tackle social difficulties at their roots.

Previously, early psychosis has been associated with reduced trust towards others. However, in an important difference from patients with a long-standing illness, patients in the early phase of the illness have been found able to overcome initial distrust during repeated social interactions with trustworthy, cooperative others. This finding shows that the capacity to build trust through positive experiences with others is retained (Fett et al., 2016; Lemmers-Jansen et al., 2018) and could suggest an intact sensitivity to social reward. Alternatively, other compensatory cognitive mechanisms may be operating to counteract deficits in trust that are due to impaired social reward sensitivity (Brüne et al., 2011). One possible cognitive mechanism is ToM. Some studies show that ToM is still relatively preserved in adolescents in the early stages of the psychotic illness (Achim et al., 2012; Korver-Nieberg et al., 2013; Ho et al., 2015; Canty et al., 2017; Bartholomeusz et al., 2018). Despite this, the findings of Bartholomeusz et al. (2018) on neural processing differences in regions related to ToM suggest that subtle changes in neural mechanisms may precede overt behavioural change in ToM.

We used an interactive trust game with a trustworthy, cooperative and not trustworthy, unfair partner during functional magnetic resonance imaging (fMRI) in a sample of 22 patients with early psychosis and 25 controls. We hypothesised that we would see lower basic trust (first investment) in patients compared with controls, but similar levels of average trust towards the game partners. Based on the hypothesis that aberrant dopaminergic signalling in response to social reward underlies psychosis and emerging social impairment, we expected to see reduced activation in the right caudate. Given the unimpaired response to cooperative behaviour, we hypothesised that compensatory processing would occur through ToM and be reflected in increased activation in associated brain regions (rTPJ and mPFC). In line with the hypothesised link between social reward sensitivity, paranoia, and social motivation, we expected associations between higher positive symptoms (particularly paranoid ideation) and negative symptoms with lower trust towards others and with reduced caudate activation.

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