Mapping structural covariance networks of facial emotion recognition in early psychosis: A pilot study
Introduction
Social cognition is defined as the mental processes involved in understanding, observing, and interpreting information in one's social environment. Research has established that people with psychosis show difficulties in social cognition, most prominently in recognizing facial emotions (Kohler et al., 2010). These deficits are present at all stages of the illness including the first-episode (Barkl et al., 2014) and are related to poorer social and occupational functioning (Couture et al., 2006, Fett et al., 2011, Irani et al., 2012).
Functional magnetic resonance imaging (fMRI) studies in non-clinical subjects have shown that processing of emotional faces in humans activates a network of regions that includes visual (fusiform face area), limbic (amygdala), temporal-parietal, and prefrontal brain areas (Fusar-Poli et al., 2009). Evidence from lesion studies (Adolphs et al., 2000, Adolphs et al., 2003) and experiments using transcranial magnetic stimulation (Pitcher et al., 2008) have demonstrated that the face region of the right somatosensory cortex is also critical for accurate facial emotion recognition. A growing literature indicates that people with psychosis show abnormal activation in these brain regions when making judgements about facial emotional expressions, and these deviant activation patterns are thought to contribute to impairments in recognizing facial emotions (Gur et al., 2007, Li et al., 2010, Pinkham et al., 2011). However, the relationship between facial emotion recognition ability and neural structure in people with psychosis is largely understudied, and should be investigated using sophisticated imaging analyses and at differing illness stages such as soon after the onset of a psychosis. Functional imaging data suggests that the “face network” may have developed atypically in this population, which may also be reflected in aberrant structure or structural networks.
Recent developments in structural imaging analyses provide an opportunity to study associations between neuroanatomy and behavioral measures, including cognition (Dziobek et al., 2010, Lerch et al., 2006). Cortical thickness measures can be extracted through a fully-automated measurement of magnetic resonance (MR) images at a subvoxel resolution, and are believed to primarily reflect morphometric gray matter features such as the size, density or arrangement of cells. (Lerch and Evans, 2005, Parent and Carpenter, 1995). Structural covariance analysis of MR-based cortical thickness data can be used to further map inter-regional anatomical networks. This approach allows measurement of cortical thickness/gray matter volume in which areas of the cortex correlate with one another, allowing evaluation of anatomical relationships in the context of large-scale networks. Covariations in gray matter are thought to result from mutually trophic and maturational influences, and have been shown to partially reflect underlying white matter tracts and functional connectivity networks (Alexander-Bloch et al., 2013, Mechelli et al., 2005, Raznahan et al., 2011). A combined approach involving cortical thickness and structural covariance network analyses has the potential to provide information about underlying patterns of structure and network relationships that are associated with facial emotion recognition abilities in people with psychosis, which is lacking in the current literature.
The aims of the current study were fourfold. Our first aim was to compare cortical thickness in an early psychosis sample to a historical control group. In line with meta-analytic results (Bora et al., 2011) we hypothesized reduced cortical thickness in early psychosis subjects compared to controls in frontal and temporal regions. Our second aim was to assess structural covariance within intrinsic networks of facial emotion recognition, using the right somatosensory cortex (Pitcher et al., 2008) and bilateral fusiform face areas (Fusar-Poli et al., 2009) as seed regions of interest, in early psychosis subjects vs. controls. We hypothesized that early psychosis subjects would show alterations in network properties compared with controls. Our third aim was to evaluate associations between facial emotion recognition and cortical thickness across the cortical mantle in the early psychosis group, using the right somatosensory cortex and bilateral fusiform face regions as seeds. In line with functional imaging data showing that poorer facial emotion abilities are associated with altered activation in widespread cortical regions in this population (Gur et al., 2007), we hypothesized that early psychosis subjects would show different patterns of associations between cortical thickness and facial emotion recognition ability than controls. Our fourth aim was to evaluate the modulation of facial emotion recognition on structural covariance between thickness in right somatosensory cortex and bilateral fusiform face area seeds and thickness across the brain in early psychosis subjects. Given the limited published research on structural covariance analyses, aim four was exploratory and no hypothesis was put forth.
Section snippets
Participants
Fifteen participants with a early psychosis were recruited through the Early Psychosis Treatment Service at Foothills Hospital in Calgary, Alberta, Canada, and all provided MR scans. For this study an early psychosis was defined as being within the first 3 years of receiving an initial diagnosis of psychosis, which was confirmed through chart records. Exclusion criteria were history of neurological disorder, loss of consciousness for more than 5 min, or presence of metal in the body. Twelve
Sample characteristics
Table 1 displays demographic characteristics of the early psychosis and historical control samples, as well as mean ER40 and EDF40 total accuracy scores of the early psychosis group. Control subjects had significantly greater years of education and number of females than early psychosis subjects.
Group differences in cortical thickness
Surface-based measurement of cortical thickness revealed that early psychosis subjects showed significantly thinner cortex in a cluster in the right frontal cortex encompassing the orbitofrontal, medial
Discussion
In the current study, our early psychosis subjects showed thinner cortex in right orbitofrontal cortex extending into the medial and middle frontal gyri compared to controls. Group differences in seed-based structural MRI covariance showed that early psychosis subjects showed reduced covariation between thickness in the right fusiform face region and thickness in right orbitofrontal cortex compared to controls. In early psychosis subjects, facial emotion recognition ability was not
Conflict of interest
All authors declare no conflict of interest.
Contributors
The first author performed behavioral and imaging analysis and wrote the first version of the manuscript. The second and sixth authors assisted in data collection and organization. The third author assisted with imaging analyses. The fourth and fifth authors assisted in conceptualizing the study. The seventh author oversaw the project from conception to completion and was responsible for all clinical components. All authors have contributed to the writing of the manuscript and approved the
Role of the funding source
The Mathison Centre had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.
Acknowledgements
This study was supported by a Mathison Centre Pilot Research Fund Program awarded to Jean Addington, Signe Bray and Frank McMaster. Lisa Buchy is supported by a CIHR fellowship; Mariapaola Barbato is supported by a Mathison Centre postdoctoral fellowship; Carolina Makowski is supported by an FRSQ studentship. The authors thank staff at Seaman's Family MR Research Centre for assistance with data collection. We are thankful for all the people who participated in the study.
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