Face emotion processing is a complex sensory task requiring extraction of configural information from a distributed network of features (eg, eyes, mouth, cheeks, corner of nose) in order to reach a categorical decision regarding another person’s internal state. Over recent years, deficits in early sensory processing have become increasingly well documented,37,39,44,76,87–90
particularly involving the magnocellular visual system. The present study demonstrates specific contributions of impaired early sensory processing to face emotion recognition deficits in schizophrenia.
Two experiments were performed. In experiment 1, subjects performed 2 face emotion processing tasks, the ER-40 which includes 4 emotions plus neutral faces and EMODIFF in which participants distinguish between levels of emotional expression for happy and sad faces,24,79,91
along with contrast sensitivity to low-, medium-, and high-SF stimuli. In the ER-40, patients showed deficits across all emotions except for happy, where ceiling level performance was observed for both groups. In the EMODIFF, deficits were observed in discrimination of both happy and sad emotions, with greater deficits in discriminating intensities of happy. Thus, while patients are not as impaired in identifying happy faces as for other emotions, they have greater deficits in differentiating intensities of happy.
Consistent with several prior reports, patients also showed impaired contrast sensitivity to LSF, but not HSF, stimuli,76,89
although other studies have also found HSF deficits.92,93
The current study supports the concept of a magnocellular deficit with less of a deficit in parvocellular function in schizophrenia. Furthermore, deficits in magnocellular-biased LSF contrast sensitivity correlated significantly with performance on the ER-40 and EMODIFF tasks. Even when nonspecific correlations due to group effects were considered, contrast sensitivity at 0.5 cycles/degree remained a significant predictor of emotion processing on the EMODIFF task.
Similar findings were obtained by Norton et al,26
who found that contrast sensitivity at an SF of 2 cycles/degree was related to fear recognition. The present study extends these findings across a range of emotions and demonstrates as well relative specificity for LSF vs HSF gratings, suggesting preferential magnocellular involvement.
Experiment 2 examined the pattern of emotional performance across contrast levels in schizophrenia. Although SF can be used to bias processing toward the magnocellular vs parvocellular pathways, considerable overlap may also be observed across pathways.55
A potentially more effective method for distinguishing visual systems is through manipulation of contrast.
In general, magnocellular neurons are sensitive to much lower levels of contrast than parvocellular neurons, which do not begin to respond until contrast levels reach approximately 10%.64
In addition, responses of magnocellular neurons saturate above approximately 16% contrast, whereas parvocellular neurons show continued increase in response as contrasts increase from approximately 16% to 100%. In ssVEP studies, therefore, the 2 systems can be studied independently by examining contrast response functions in which stimuli appear and disappear, which yields a typical nonlinear magnocellular response curve (), or by modulating contrasts around a high standing level of contrast, which yields a more linear nonsaturating curve typical of parvocellular neurons ().55,61,63
As in prior ssVEP studies, patients showed significant reduction in plateau level of the magnocellular, with relatively preserved parvocellular, response.76,84
The nonlinear response pattern in the magnocellular-biased condition reflects both amplification of the responses at low contrast by nonlinear circuit elements, such as NMDA-type glutamate receptors, and divisive gain at higher contrast (ie, neurons are inhibited due to local GABAergic feedback within primary visual regions).35
As with other neurophysiological deficits in schizophrenia, impaired ssVEP generation, therefore, may reflect either decreased excitatory drive through NMDA receptors or altered GABAergic feedback.87,94
Preferential magnocellular dysfunction in schizophrenia may reflect impaired nonlinear gain, with parvocellular dysfunction seen when the parvocellular system is driven into a more nonlinear gain process.76
The present study is the first to evaluate patterns of emotion-processing deficits across a range of contrasts. Both groups showed high sensitivity even at relatively low contrasts with saturation in performance above 8% contrast, suggesting that, at least for emotions tested here, the information required for emotion discrimination can be carried primarily by the magnocellular system, with little additional benefit obtained from the more highly detailed information provided by parvocellular input. In addition, impairments in face processing correlated significantly with impaired generation of magnocellular-based, but not parvocellular-based, ssVEP responses, and with reduced contrast sensitivity to LSF, but not HSF, stimuli, supporting preferential magnocellular involvement in face emotion processing.
In the present study, deficits in emotion recognition were also observed across a range of emotions, supporting generalized sensory deficits rather than deficits in specific emotion circuits. For example, with amygdala damage, such as with the well-described subject SM,95
patients have selective deficits in detection of fear based upon impaired scanning of eyes. The absence of a selective deficit in the present study argues against preferential amygdala involvement, although contributions of impaired amygdala function to the overall pattern of deficit cannot be excluded.
Conscious awareness of stimuli is mediated primarily based upon activity within ventral stream structures, such as lateral occipital complex,96
which receive predominant input from the parvocellular system, whereas activity in dorsal stream does not typically reach consciousness. Consequently, schizophrenia patients would not necessarily be consciously aware of magnocellular dysfunction nor would they show impairments on routine assessments of visual function such as eye charts, which test primarily ventral stream object recognition-type functions. Nevertheless, the magnocellular system provides a crucial organizing input that permits the brain to make rapid assessments of potential object identity53
and to control eye movements to efficiently explore the visual space.97,98
Deficits in magnocellular function thus contribute to impairments in a range of complex visual tasks such as fragmented object recognition,48
Seen from this perspective, face emotion recognition is merely a complex visual task in which disparate information must be extracted from a complex visual stimulus using an efficient search approach.101
In this study, all patients were on antipsychotic medication raising the issue of a potential medication effect. However, emotion processing as well as visual processing deficits are also found in unmedicated first-degree family members77,102
and in the present study no significant correlations were found with CPZ equivalents. The majority of the patients tested were inpatients. Future studies will address effects of sensory processing deficits on emotion dysfunction in outpatients as well as at different stages of illness.
Face emotion recognition, along with auditory emotion recognition, are hallmarks of the construct of social cognition. We have over the past several years documented significant contributions of impaired early auditory processing, such as inability to detect pitch modulations, to voice emotion recognition.103,104
The present study thus suggests that the severe impairments in social cognition in schizophrenia may result from a “perfect storm” in which signals needed for emotion detection are deficient in both the auditory and the visual modalities, leaving subjects diminished opportunity to compensate for the combined deficit.
Determining the neural basis for emotion-processing deficits helps clarify their mechanism and contribution to impaired outcome in schizophrenia. Demonstrating the relationship with sensory processing deficits is critical for several reasons. First, it underscores that patients are not inherently nonemotional. As shown in various evocative studies, patients experience similar amounts of pleasant and unpleasant emotions as controls.2,14,15,17,32–34
Second, even if sensory deficits are generally not treated at present, understanding their contribution to impaired social cognition may assist patients, families, and caregivers in defining compensatory strategies. Perhaps most importantly, present results highlight the need for remediation of basic sensory deficits in schizophrenia (see Adcock et al105
, this volume) and suggest that such approaches may be critical for restoration of social function.