Motivation and Pleasure Deficits Undermine the Benefits of Social Affiliation in Psychosis

Abstract

In psychotic disorders, motivation and pleasure (MAP) deficits are associated with decreased affiliation and heightened functional impairment. We leveraged a transdiagnostic sample enriched for psychosis and a multi-method approach to test the hypothesis that MAP deficits undermine the stress-buffering benefits of affiliation. Participants completed the Social Affiliation Enhancement Task (SAET) to cultivate affiliation with an experimental partner. Although the SAET increased perceived affiliation and mood, individuals with greater negative symptoms derived smaller emotional benefits from the partners, as indexed by self-report and facial behavior. We then used the Handholding fMRI paradigm, which combines threat-anticipation with affiliative physical contact, to determine whether MAP deficits undermine the social regulation of distress. Individuals with greater MAP deficits showed diminished neural 'benefits'-reduced dampening of threat-elicited activation-from affiliative touch in key frontoparietal nodes of the Dorsal Attention Network. In short, MAP symptoms disrupt the emotional and neuroregulatory benefits of affiliation.

Keywords: anhedonia/avolition; interpersonal emotion regulation; negative symptoms; psychosis/psychotic spectrum; schizophrenia; social affiliative deficits; social baseline theory.

Figure 1. Conceptual Overview of the Two-Phase Laboratory Assessment

a. The Social Affiliation Enhancement Task (SAET). In the first phase of the session, participants completed the SAET, which encompasses 3 tasks—Conversation, Implicit Fingertip Synchrony, and Team Building. b. The Handholding fMRI paradigm. In the second phase of the session, participants completed the Handholding fMRI paradigm. In each scan, participants held the hand of the experimental partner, a stranger, or no one (‘Alone’). Each scan included an event-related cued threat-anticipation task. To elicit robust anxiety, Threat trials (red) were variable in duration and culminated in the presentation of negative reinforcers (p=.50) or neutral reinforcers (p=.50). Safe trials (blue) were fixed duration (mean duration matched across conditions), and culminated in neutral reinforcers (p=1.0). Negative reinforcers included a noxious electric shock, aversive auditory clip, and a photograph of an angry or fearful face. Neutral reinforcers included a just-perceptible electrical pulse, neutral auditory clip, and a photograph of a neutral face. The bottom-right panel depicts an example of the trial structure and the expected hemodynamic responses to Threat anticipation (red trace), negative reinforcers (yellow trace), and neutral reinforcers (green trace) for a representative scan. Subjects completed up to 6 scans in total (2 scans/handholding condition). Abbreviation—SAET=Social Affiliation Enhancement Task.

Figure 2. Motivation and Pleasure Deficits Undermine the Neural Benefits of Social Affiliation

a. Threat anticipation. A whole-brain voxelwise GLM confirmed that Threat (relative to Safe) anticipation was associated with significant activation in regions previously implicated in the expression and regulation of fear and anxiety (p<0.05, whole-brain corrected for cluster extent). b-c. MAP deficits reduce partner handholding benefit. A whole-brain voxelwise regression was used to identify regions where the degree of handholding ‘benefit’ co-varied with clinician-rated MAP symptoms. Results revealed significant clusters in the left FEF, IPS, and SMG (p<0.05, whole-brain corrected; Supplementary Table S4). d. SMG. e. FEF. f. IPS. Blue circles represent cases. Solid red line indicates the OLS regression slope. Broken orange line indicates the robust regression slope. Purple humps along the axes depict the smoothed density distributions for each variable. Abbreviations—CAINS=Clinical Assessment Interview for Negative Symptoms; FEF=putative human Frontal Eye Field region; IPS=Intraparietal Sulcus; MAP=Motivation and Pleasure; OLS=Ordinary Least-Squares regression; SMG=Supramarginal Gyrus (Parietal Cortex).