Psychologists and cognitive neuroscientists have often found it useful to fractionate cognitive processes into sensory-perceptual components and evaluative–executive components. While most cognitive processes, such as affective appraisal, undoubtedly result from the interaction of both components, isolating the neural underpinnings of these components can prove challenging in neuroimaging experiments. For clinical neuroscientists who wish to identify the locus of a specific neurocognitive abnormality, examining processes such as facial affect in terms of evaluative and executive processing vs
sensory and perceptual processing can be especially informative. Within schizophrenia, a leading hypothesis attributing neurocognitive deficits to dopaminergic-based hypofrontality favours evaluative and executive explanations (Weinberger and Berman 1988
; Carter et al.
; O'Reilly et al.
; Bach et al.
; Phillips et al.
). In contrast, glutamatergic (Javitt, 1996
) or GABAergic (Lewis and Moghaddam, 2006
) hypotheses emphasize more widespread neural dysfunction that also encompasses basic sensation and perception processes. Studies exploiting the high temporal resolution of event-related potentials (ERP) have indicated that facial affect perception is associated with reductions in early visuosensory components such as P1 and N1, while other studies found reductions only for latter stage ‘integration’ components such as the N170 and N250 (see Turetsky et al.
for review). The presence of early ERP abnormalities in schizophrenia suggests basic sensory deficits, without ruling out the possibility that additional evaluative–executive deficits also contribute to impairment in facial affect identification. Studies by Van’t Wout and colleagues (2007
) show that patients’ recognition of emotions such as fear is significantly impaired in explicit but not implicit emotion processing tasks. This disjunction suggests that task demand and affective evaluation may reflect impairment beyond pure sensory encoding of faces and their expressions. Similarly, studies by Green and colleagues (2007
) examining gaze direction patterns have suggested that patients have difficulty integrating contextual information when making emotional and social judgments. Such affective evaluative impairment may reflect a more general executive impairment in utilizing context that has been long linked to frontal hypofunction (e.g. MacDonald et al.
The low temporal resolution of fMRI can make it difficult to disentangle relative contributions of sensory and executive processing abnormalities to affective appraisal. However, the current study’s hybrid (block and event-related) design afforded us the opportunity to examine evaluation aspects of face processing while holding sensory and perceptual effects (stimulus characteristics) constant. We compared identical faces that were foils in an emotion identification experiment under differing task demand contexts, hypothesizing that blocked trials in which subjects were asked to detect happy and sad emotions would form an AFcontext, while anger and fear target blocks would form a TH context. Prior research into the effects of context on affective evaluation had implicated VLPFC and OFC brain regions (Haxby et al.
; Mobbs et al.
; Guyer et al.
), hence we focused our analysis on this system.
Our finding of reduced ventral PFC activation to foils in schizophrenia is consistent with prior studies of affective appraisal, and more general findings of hypofrontality in the illness. Consistent with our hypothesis, we found that incongruent AF foils in the context of TH conditions produced less efficient behavioural responses and also elicited greater bilateral activation in VLPFC–OFC compared with their identical context-congruent counterparts. These finding suggest that task demands of TH detection exert significant contextual effects on affective evaluation. Within RH, this context modulation was present in healthy subjects but not in schizophrenia patients. Behaviourally, patients showed a nearly 2-fold greater reduction in efficiency than healthy subjects within the AFTHcontext − AFTHcontext contrast. Together, these behaviour and imaging findings illustrate abnormal evaluative processing deficits that are likely not directly attributable to sensory integration deficits. Both behavioural and activation effects were not related to medication dosage, indicating no direct role of antipsychotic medication on the observed context effects. Finally, in the patient group, reduced modulation of VLPFC–OFC activation to TH foils by incongruent vs congruent context was associated with greater affective flattening. Although no overall group differences were seen in this TH foil contrast, the symptom correlation suggests that patients with flat affect may be less likely to effectively employ contextual cues when appraising threatening facial stimuli under AF conditions.
A post hoc whole brain analysis (Supplementary Figure 1
) of activation to AF foils in an incongruent TH context (AFTHcontext
activation to identical AF foils in a congruent AF context (AFAFcontext
) revealed only two clusters that reached our statistical significance criteria. These clusters substantially overlapped with our a priori VLPFC/OFC ROI, yet the activation also extended to more dorsal aspects of PFC. In contrast, patients displayed only slight and subthreshold activation clusters in this contrast. No significant difference in activation was observed in the THAFcontext vs
contrast within either group.
This study highlights the interpretative limitations of block designs, which are commonly employed in examining facial affect in clinical populations. Blocks with different task demands may induce context effects that alter response to otherwise identical stimuli, and group differences in block activation could reflect either context or stimulus effects. Thus, abnormal activation in schizophrenia during block-design tasks could reflect higher level deficits in context processing, while typically being interpreted as differences in response to stimulus features.
Our analysis of affective foils indicated that patients had reduced activation within our ROI to facial stimuli in general. This is consistent with prior work suggesting that schizophrenia patients have core deficits in face perception that extend beyond affective appraisal (Hooker and Park 2002
; Leitman et al.
). The presence of these deficits in our sample indicate that despite our comparison of identical stimuli under differing contexts, we cannot completely rule out the possibility that the absence of context effects on the appraisal of AF stimuli seen in patients reflects an interaction between stimulus-driven sensory dysfunction and controlled evaluative processing deficits. Future studies directly accounting for differences in sensory–perceptual processing will be needed to settle this question definitively.
There are several limitations to our study. Task demands in the current study likely produce only weak contextual effects. Stronger contextual effects, such as those imposed in ‘correspondence bias’ and contextual framing paradigms, may induce even more robust changes in VLPFC/OFC. No significant difference within this ROI was found for incongruent TH foils in AF blocks vs
their identical congruent counterparts. This disjunction suggests that TH-detection task demands create stronger contextual effects than those produced by task demands emphasizing affiliation. It is also possible that anger and fear are more closely aligned dimensionally in terms of TH than happiness and sadness are in terms of affiliation. Future studies should look at each emotion separately to explore emotion-specific contextual effects. Functional connectivity analysis could also help examine how context modulates interactions between frontal evaluative regions, amygdala and other neural nodes in the affective appraisal circuit. We did not directly assess subjective emotional responses to face stimuli, so we cannot rule out the possibility that patients experiences of stimuli as AF or threatening may vary somewhat from control subjects. We think this is unlikely to explain our context results, as prior studies indicate that schizophrenia patients have qualitatively similar subjective emotional responses to laboratory emotional stimuli (Kring et al.
; Kring and Neale, 1996
); however, future studies should directly assess the afiliative vs
threatening judgments in patients.
In daily life, affective appraisal takes place within situational contexts. Such contextual effects substantially shape memory encoding and recall, in some cases dramatically (Loftus and Pickrell, 1995
; Loftus and Mazzoni, 1998
). Context can also alter the perceptual threshold of stimuli, rendering detectable previously subthreshold stimuli (Cox et al.
; Bar et al.
). Such contextual information impacts directly on affect appraisal through executive control linked to VLPC–OFC (Haxby et al.
; Adolphs, 2002
). Executive processing may facilitate affective appraisal by improving the efficiency and accuracy of TH prediction, for example, by constraining search within memory systems (Sahakyan and Kelley, 2002
; Mobbs et al.
). Our study documented task-driven contextual effects on VLPFC–OFC processing of facial affect that were reduced in patients with schizophrenia. This suggests that patients may have difficulty utilizing prefrontal control mechanisms that optimize affective appraisal.