Blunted Ventral Striatal Reactivity to Social Reward Is Associated with More Severe Motivation and Pleasure Deficits in Psychosis

Abstract

Background and hypothesis: Among individuals living with psychotic disorders, social impairment is common, debilitating, and challenging to treat. While the roots of this impairment are undoubtedly complex, converging lines of evidence suggest that social motivation and pleasure (MAP) deficits play a central role. Yet most neuroimaging studies have focused on monetary rewards, precluding decisive inferences.

Study design: Here we leveraged parallel social and monetary incentive delay functional magnetic resonance imaging paradigms to test whether blunted reactivity to social incentives in the ventral striatum-a key component of the distributed neural circuit mediating appetitive motivation and hedonic pleasure-is associated with more severe MAP symptoms in a transdiagnostic adult sample enriched for psychosis. To maximize ecological validity and translational relevance, we capitalized on naturalistic audiovisual clips of an established social partner expressing positive feedback.

Study results: Although both paradigms robustly engaged the ventral striatum, only reactivity to social incentives was associated with clinician-rated MAP deficits. This association remained significant when controlling for other symptoms, binary diagnostic status, or striatal reactivity to monetary incentives. Follow-up analyses suggested that this association predominantly reflects diminished activation during the presentation of social reward.

Conclusions: These observations provide a neurobiologically grounded framework for conceptualizing the social-anhedonia symptoms and social impairments that characterize many individuals living with psychotic disorders and underscore the need to develop targeted intervention strategies.

Keywords: fMRI; incentive delay paradigm; negative symptoms; psychosis/psychotic spectrum; schizophrenia; social anhedonia/avolition.

Figure 1.

The Human Ventral Striatum. The Ventral Striatum Includes the Nucleus Accumbens and Olfactory Tubercle. The Accumbens Can, in Turn, be Chemoarchitectonically Divided Into 2 Major Divisions, the Shell and Core, With the Shell Marked by Stronger Expression of Mu and Kappa Opioid Receptors and D1 and D3 Dopamine Receptors, and Weaker Expression of D2 Dopamine Receptors.^, Mechanistic Work in Rodents Indicates That Both Divisions are Critically Involved in Dopamine-Mediated Appetitive Motivation (“wanting” Reward), Whereas Only the Medial Shell is Involved in Opioid/Cannabinoid-Mediated Hedonic Pleasure (“liking” Reward).^, The Figure was Created with Reference to the Allen Institute and Mai atlases.^, Abbreviations: GP, Globus Pallidus; NACc, Nucleus Accumbens Core; NACs, Nucleus Accumbens Shell; OT, Olfactory Tubercle.

Figure 2.

Conceptual Overview of the Study. (a) Pre-Scan 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—Aimed at Promoting a Sense of Affiliation with an Experimental Partner. Prior Work Confirms the Validity of this Approach in Psychotic Samples. (b) Social and Monetary Incentive Delay (SID/MID) fMRI Paradigms. (c) Naturalistic Audiovisual Outcomes. To Maximize Ecological Validity and Translational Relevance, Short Audiovisual Clips Depicting Varying Degrees of Social or Monetary Reward Served as the Outcomes. For the SID Paradigm, the Clips Depicted the Individual Who Served as the Experimental Partner During the SAET. Staff Carefully Assessed Task Comprehension Prior to Scanning. Participants Were Fully Aware That the Clips Were Pre-Recorded. (d) Voxelwise Hypothesis Testing. Hypothesis Testing Focused on the Association between Clinician-Rated MAP Symptoms and Ventral Striatum Reactivity to Social and Monetary Reward, Indexed by the Cardinal High-Reward vs. No-Reward Contrast. Analyses Focused on Trials Where the Participant Responded Sufficiently Fast to Earn Reward (“hit”). For Primary Hypothesis Testing, Each Condition Was Modeled Using a Rectangular Function Spanning the Entire Trial. Abbreviations: fMRI, Functional Magnetic Resonance Imaging; MAP, Motivation and Pleasure; MID, Monetary Incentive Delay Paradigm; ms, Milliseconds; RT, Response Time; SID, Social Incentive Delay Paradigm.

Figure 3.

Social and Monetary Incentives Both Robustly Engage the Ventral Striatum. Figure Depicts Regions Showing Significantly Greater Activation During High-Reward Compared With No-Reward Hit Trials for the SID (Left) and MID (Right) paradigms (P < .05, Whole-Brain FWE Corrected). Each Condition was Modeled Using a Rectangular Regressor Spanning the Entire Trial. Arrows Indicate the Ventral Striatum. For detailed results, see Supplementary Tables S2–S5. Abbreviations: FWE, Familywise Error; L, Left Hemisphere; WB, Whole-Brain.

Figure 4.

Blunted Ventral Striatum Reactivity to Naturalistic Social Incentives is Associated With More Severe Clinician-Rated MAP Deficits. (a) Decreased Ventral Striatum Activation During High-Reward SID Trials is Associated With More Severe MAP Symptoms. The Peak Lies in the Region of the Medial Shell of the Nucleus Accumbens (x = −4, y = 6, z = −8; cf. Figure 1). (b) Decreased Activation During the Presentation Phase of High-Reward SID Trials is Associated With More Severe MAP Symptoms in an Overlapping Region of the Ventral Striatum (red) (x = −4, y = 6, z = −8). Red lines depict the regression slope for the peak voxel. Gray envelopes depict 95% confidence intervals. Dots and ticks indicate individual participants. Analyses controlled for mean-centered age and biological sex (P < .05 FWE corrected for the volume of the anatomically defined ventral striatum). Key conclusions remained unchanged for analyses employing robust regression. Abbreviations: Corr., Corrected for the Volume of the Anatomically Defined Ventral Striatum; FWE, Familywise Error; MAP, Motivation-and-Pleasure Symptoms (CAINS); NAC, Nucleus Accumbens; SID, Social Incentive Delay Paradigm.