Insular and Striatal Correlates of Uncertain Risky Reward Pursuit in Schizophrenia

Abstract

Background and hypothesis: Risk-taking in specific contexts can be beneficial, leading to rewarding outcomes. Schizophrenia is associated with disadvantageous decision-making, as subjects pursue uncertain risky rewards less than controls. However, it is unclear whether this behavior is associated with more risk sensitivity or less reward incentivization. Matching on demographics and intelligence quotient (IQ), we determined whether risk-taking was more associated with brain activation in regions affiliated with risk evaluation or reward processing.

Study design: Subjects (30 schizophrenia/schizoaffective disorder, 30 controls) completed a modified, fMRI Balloon Analogue Risk Task. Brain activation was modeled during decisions to pursue risky rewards and parametrically modeled according to risk level.

Study results: The schizophrenia group exhibited less risky-reward pursuit despite previous adverse outcomes (Average Explosions; F(1,59) = 4.06, P = .048) but the comparable point at which risk-taking was volitionally discontinued (Adjusted Pumps; F(1,59) = 2.65, P = .11). Less activation was found in schizophrenia via whole brain and region of interest (ROI) analyses in the right (F(1,59) = 14.91, P < 0.001) and left (F(1,59) = 16.34, P < 0.001) nucleus accumbens (NAcc) during decisions to pursue rewards relative to riskiness. Risk-taking correlated with IQ in schizophrenia, but not controls. Path analyses of average ROI activation revealed less statistically determined influence of anterior insula upon dorsal anterior cingulate bilaterally (left: χ2 = 12.73, P < .001; right: χ2 = 9.54, P = .002) during risky reward pursuit in schizophrenia.

Conclusions: NAcc activation in schizophrenia varied less according to the relative riskiness of uncertain rewards compared to controls, suggesting aberrations in reward processing. The lack of activation differences in other regions suggests similar risk evaluation. Less insular influence on the anterior cingulate may relate to attenuated salience attribution or inability for risk-related brain region collaboration to sufficiently perceive situational risk.

Keywords: Psychosis; cingulate; decision-making; fMRI; nucleus accumbens; risk-taking; schizoaffective disorder.

Fig. 1.

Correlations between intelligence quotient (IQ), risk-taking, and NAcc activation. Top: Adjusted pumps are average inflations on unexploded balloons. Average explosions per task run. Middle: IQ and risk-taking scatter plots. Bottom: IQ, risk-taking, and NAcc activation correlations. ^†indicates correlations surviving Bonferroni correction for 6 analyses.

Figure 2.

Whole-brain activation clusters in the striatum and insula during decisions to pursue risky rewards relative to risk (ChooseInflate_pmod).

Fig. 3.

Path analysis results during risk-taking (ChooseInflate–ChooseWin). Anterior insula (AI) and nucleus accumbens regions of interest (ROIs) were unilateral. Anterior cingulate ROI was bilateral. Numbers left of the arrows reflect left hemisphere path coefficients and numbers on the right reflect right hemisphere coefficients. Blue/Left: controls. Red/Right: schizophrenia group.