Anhedonia and emotional experience in schizophrenia: neural and behavioral indicators

Abstract

Background: Emotional impairments such as anhedonia are often considered key features of schizophrenia. However, self-report research suggests that emotional experience in response to affect-eliciting stimuli is intact in schizophrenia. Investigation of neural activity during emotional experience may help clarify whether symptoms of anhedonia more likely reflect alterations of in-the-moment hedonic experience or impairments in other aspects of goal-directed behavior.

Methods: Forty individuals with DSM-IV-TR schizophrenia or schizoaffective disorder and 32 healthy control subjects underwent functional magnetic resonance imaging while making valence and arousal ratings in response to emotional pictures, words, and faces. Blood oxygen level-dependent responses were compared between patients and control subjects and were correlated with questionnaire measures of anhedonia.

Results: Patients showed some evidence of blunted valence but not arousal ratings in response to emotional stimuli compared with control subjects. Higher anhedonia scores were associated with blunted valence ratings in both groups and fully mediated the group differences in valence ratings. Functional activity was largely intact in patients, except for regions in right ventral striatum and left putamen, which showed reduced responses to positive stimuli. Higher anhedonia was associated with reduced activation to positive versus negative stimuli in bilateral amygdala and right ventral striatum in patients and in bilateral caudate in control subjects.

Conclusions: Increased anhedonia is associated with a reduced experience of valence in both patients and control subjects, and group differences in experienced valence are likely driven by individual differences in anhedonia. Reduced activation of the striatum and amygdala may contribute to symptoms of anhedonia by failing to signal the salience of positive events.

Figure 1

Valence and arousal ratings as a function of condition in individuals with schizophrenia (SCZ) and controls (CON). (a) Average valence ratings (1=negative, 2=neutral, 3=positive) collapsed across stimulus type (pictures, words, faces) for each emotional condition: negative high arousal (NHA), negative low arousal (NLA), neutral (NEU), positive low arousal (PLA), and positive high arousal (PHA). (b) Average arousal ratings (1=highly aroused, 2=slightly aroused, 3=not aroused) collapsed across stimulus type (pictures, words, faces) for each emotional condition. * p < .05. Error bars represent standard error.

Figure 2

Scatterplots of (a) average valence ratings to positive high arousal (PHA) stimuli as a function of Chapman physical anhedonia, (b) average valence ratings to positive high arousal (PHA) stimuli as a function of Chapman social anhedonia, (c) average valence ratings to negative high arousal (NHA) stimuli as a function of Chapman physical anhedonia, and (d) average valence ratings to negative high arousal (NHA) stimuli as a function of Chapman social anhedonia, in individuals with schizophrenia (SCZ; circles) and controls (CON; triangles).

Figure 3

Results of ROI analyses of valence, arousal, and valenceXarousal contrasts in the total sample (both patients and controls). Regions are described in Table 3. Images are shown in neurological orientation. (a) Regions showing significant activation in the valence contrast. Positive z-scores (red) indicate greater activation to positively valenced stimuli than to negatively valenced stimuli; negative z-scores (blue) indicate greater activation to negatively valenced stimuli than to positively valenced stimuli. (b) Regions showing significant activation in the arousal contrast. Positive z-scores (red) indicate greater activation to high arousal stimuli relative to neutral and low-arousal stimuli. (c) Regions showing significant activation in the valence-by-arousal contrast. Negative z-scores indicate greater activation to negative high arousal stimuli than to positive and/or low-arousal stimuli.

Figure 4

Results of ROI analyses of group t-tests between patients and controls for the valence and valenceXarousal contrasts. Regions are described in Table 4. Images are shown in neurological orientation. (a) Right ventral striatal region demonstrating a group difference in the valence contrast. Activation did not differ significantly in the negative high arousal (NHA), negative low arousal (NLA), or neutral (NEU) conditions, but was significantly lower in patients than in controls for the positive low arousal (PLA) and positive high arousal (PHA) conditions. (b) Left putamen region demonstrating a group difference in the valenceXarousal contrast. Activation did not differ significantly in the negative, neutral, or PLA conditions, but was significantly lower in patients than in controls in the PHA condition. * p < .05. Error bars represent standard error.

Figure 5

Results of whole-brain analyses of valence, arousal, and valenceXarousal contrasts in the total sample (both patients and controls). Regions are described in Table 5. Images are shown in neurological orientation. (a) Regions showing significant activation in the valence contrast. Positive z-scores (red) indicate greater activation to positively valenced stimuli than to negatively valenced stimuli; negative z-scores (blue) indicate greater activation to negatively valenced stimuli than to positively valenced stimuli. (b) Regions showing significant activation in the arousal contrast. Positive z-scores (red) indicate greater activation to high arousal stimuli relative to neutral and low-arousal stimuli; negative z-scores (blue) indicate greater activation to neutral and low-arousal stimuli than to high-arousal stimuli. (c) Regions showing significant activation in the valenceXarousal contrast. Negative z-scores indicate greater activation to negative high arousal stimuli than to positive and/or low-arousal stimuli.