Neural correlates of dynamic emotion perception in schizophrenia and the influence of prior expectations
Introduction
Emotion perception is impaired in schizophrenia (SCZ) with a significant impact on overall functional outcome (Irani et al., 2012). Currently, there is inadequate knowledge of the cognitive and neural processes underlying emotion perception difficulties in SCZ. The ‘Predictive Coding’ theory of perception proposes that our brain continually generates predictive models of the world, based on prior expectations (generated from previous experiences) and new sensory information (Friston and Kiebel, 2009; Friston et al., 2006). Under this theory, emotional information that is congruent with prior expectations is processed more efficiently, as prior expectations direct attentional focus and decrease processing resources (Barbalat et al., 2013; Brown and Brune, 2012). For example, prior expectations have been found to improve speed and accuracy during emotion discrimination in healthy individuals (Barbalat et al., 2013; Dzafic et al., 2016). Within the Predictive Coding theory, SCZ has been conceptualized as a disorder of aberrant precision (certainty) in prior expectations (Sterzer et al., 2018). However, there is conflicting evidence whether patients with SCZ have reduced (Adams et al., 2016; Chambon et al., 2011; Dima et al., 2010) or increased precision in prior expectations (Alderson-Day et al., 2017; Powers et al., 2017; Teufel et al., 2015). Reduced precision in prior expectations can lead to inefficient directing of attention and nosier incoming sensory information. In contrast, increased precision in prior expectations has been implicated in psychotic experiences, such as hallucinations. In the current study, we investigated whether aberrancy in prior expectations leads to impaired recognition of dynamic, audio-visual emotion in patients with SCZ.
Processing of emotions that are congruent with prior expectations is associated with activity in frontal areas (Barbalat et al., 2013) and the amygdala (Dzafic et al., 2016). Aberrant precision in prior expectations in SCZ has been proposed to reflect impaired activity in frontal regions, resulting in aberrant inhibitory top-down influence over primary sensory regions (Adams et al., 2016). This is compatible with the considerable evidence for frontal dysfunction in SCZ (Fan et al., 2013; He et al., 2013; Huang et al., 2010) and hyper-connectivity in sensory regions (Anticevic et al., 2014). In addition to frontal dysfunction in SCZ, several converging lines of evidence have found that deficits in emotion perception are associated with dysconnectivity in functional networks involving the amygdala (Bjorkquist et al., 2016; Das et al., 2007; Mukherjee et al., 2012). However, no study to date has directly explored the neural circuitry underlying aberrant prior expectations in SCZ during emotion perception.
In summary, our aim was to investigate the influence of prior expectations on naturalistic emotion perception in SCZ, and the underlying distinct patterns of brain activity, and functional connectivity with the rAMY. The effect of prior expectations on emotion perception in SCZ has only been investigated using static emotion displays (Barbalat et al., 2012), despite that sensory information in emotional expressions is dynamic in nature and often changes rapidly in social situations. In line with previous studies (Hargreaves et al., 2016; Johnston et al., 2010) we predicted that SCZ patients would have deficits in discriminating dynamic emotion perception in general, with greater deficits compared to healthy controls when emotion perception relies on prior expectations (Chambon et al., 2011); in other words, detecting emotions congruent with prior expectations. At the neural level, we predicted reduced activation in frontal regions in patients with SCZ during emotion perception that is congruent with prior expectations (Anticevic et al., 2014; Barbalat et al., 2013). Finally, we predicted that SCZ patients would have greater difficulty using prior expectation to facilitate efficient emotion perception, as indexed by increased response times, and this would be associated with rAMY dysconnectivity.
Section snippets
Participants
Sixteen, right-handed patients with chronic SCZ (age range = 30–57; mean age = 46.40, SD = 9.43) were recruited from the Queensland Centre for Mental Health Research (QCMHR). Sixteen age and sex matched, right-handed healthy controls (HC; age range = 34–58; mean age = 45.19, SD = 7.92) were recruited from a National Health and Medical Research Council (NHMRC)-funded, population-based Australian sample of individuals as controls for the SCZ participants. The SCZ patients were comprehensively
Behavioural analyses
Discriminability was calculated using d′ scores (d′ = z(Hits) − z(False Alarms)) (Macmillan and Creelman, 1990) to assess emotion discriminability for each participant. For this calculation, we adjusted d′ according to Corwin (1994), where Hit rate = 1 or False alarm = 0. We conducted a two-way factorial ANOVA to investigate differences between SCZ and HC in discriminability for each emotional video (angry, happy, and neutral).
Mean reaction times (RTs) and accuracy percentage from all responses
Behavioural findings – emotion discriminability
A factorial ANOVA 3 (emotion video) × 2 (group) on discriminability d′ showed a significant main effect of group, F(1, 28) = 11.30, p = 0.002, indicating that SCZ have a lower discriminability compared with HC across different emotions. There was also a trend for an interaction between group and emotion, F(2, 56) = 2.65, p = 0.079 (see Fig. 1c).
Behavioural findings – prior expectations on emotion perception
A factorial ANOVA 3 (emotion video) × 2 (congruency) × 2 (group) on percentage accuracy revealed a main effect of group, F(1, 27) = 7.88, p = 0.009, SCZ
Discussion
In the current study, we investigated dynamic emotion perception in patients with SCZ and the influence of prior expectations at the behavioural and neural levels. We identified reduced ability in SCZ patients to identify emotions that were congruently cued (i.e., congruent with prior expectations), as evidenced by poorer accuracy. At the neural level, we found reduced activity in right inferior frontal gyrus (IFG) and inferior parietal lobule, as well as rAMY dysconnectivity during congruent
Funding
This work was supported by the Australian National Health and Medical Research Council [Grant number: 631671] awarded to BM.
Contributors
Author ID designed the paradigm, analysed the data and wrote the first draft of the manuscript. All authors assisted in the design of the paradigm and contributed to and have approved the final manuscript.
Conflict of interest
The authors declare no competing financial interests.
Acknowledgements
The authors thank the participants for their time and acknowledge the invaluable practical support provided by the imaging staff at the Centre for Advanced Imaging.
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