Altered activation and functional connectivity of neural systems supporting cognitive control of emotion in psychosis proneness

Abstract

Emotion regulation processes, such as reappraisal, are thought to operate through interactions between prefrontal emotion-control regions and subcortical emotion-generation regions such as the amygdala. Impairments in emotional processing and regulation have been reported in schizophrenia and at-risk populations. Psychometric measures may be used to detect vulnerability to schizophrenia in non-clinical samples, or psychosis proneness (PP). It has been shown that individuals with PP have a more than tenfold increased risk of developing a schizophrenia-spectrum disorder. In the present study, we used fMRI to examine the neural dynamics underlying reappraisal in such a sample. 600 undergraduate students completed the Community Assessment of Psychic Experiences Questionnaire (CAPE), positive subscale. Two groups were subsequently formed from the extremes of the distribution (total N=34). Blood-oxygenated-level-dependent activity elicited with a task involving 3 conditions was analyzed: viewing neutral pictures, viewing negative pictures, and reappraising negative pictures. Subjects reported the strength of experienced negative affect after each trial. Functional connectivity between prefrontal control regions and amygdala was investigated. At the behavioral level, both groups reported successful diminishment of experienced negative emotion. However, high psychosis-prone subjects showed stronger activation than low subjects in a number of prefrontal regions during reappraisal, relative to attending to negative pictures. The amygdala response to negative stimuli was decreased through reappraisal only in the low group. Functional connectivity analysis revealed less prefrontal-amygdala coupling in high psychosis-prone subjects. Thus, reduced cognitive control of emotion at a neural level appeared to be associated with PP. These findings extend the hypothesis of emotion dysregulation in schizophrenia to PP, and suggest that emotion regulation difficulties may be at the core of a vulnerability to psychosis.