Structural connections support emotional connections: Uncinate Fasciculus microstructure is related to the ability to decode facial emotion expressions

Bethany M Coad,Mark Postans,Carl J Hodgetts,Nils Muhlert,Kim S Graham,Andrew D Lawrence

doi:10.1016/j.neuropsychologia.2017.11.006

Bethany M Coad, Mark Postans + Show 4 more

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https://doi.org/10.1016/j.neuropsychologia.2017.11.006

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Journal: Neuropsychologia	Publication Date: Nov 6, 2017
Citations: 44	License type: cc-by

Affiliation: Cardiff University, University of Manchester

Abstract

The Uncinate Fasciculus (UF) is an association fibre tract connecting regions in the frontal and anterior temporal lobes. UF disruption is seen in several disorders associated with impaired social behaviour, but its functional role is unclear. Here we set out to test the hypothesis that the UF is important for facial expression processing, an ability fundamental to adaptive social behaviour. In two separate experiments in healthy adults, we used high-angular resolution diffusion-weighted imaging (HARDI) and constrained spherical deconvolution (CSD) tractography to virtually dissect the UF, plus a control tract (the corticospinal tract (CST)), and quantify, via fractional anisotropy (FA), individual differences in tract microstructure. In Experiment 1, participants completed the Reading the Mind in the Eyes Task (RMET), a well-validated assay of facial expression decoding. In Experiment 2, a different set of participants completed the RMET, plus an odd-emotion-out task of facial emotion discrimination. In both experiments, participants also completed a control odd-identity-out facial identity discrimination task. In Experiment 1, FA of the right-, but not the left-hemisphere, UF was significantly correlated with performance on the RMET task, specifically for emotional, but not neutral expressions. UF FA was not significantly correlated with facial identity discrimination performance. In Experiment 2, FA of the right-, but not left-hemisphere, UF was again significantly correlated with performance on emotional items from the RMET, together with performance on the facial emotion discrimination task. Again, no significant association was found between UF FA and facial identity discrimination performance. Our findings highlight the contribution of right-hemisphere UF microstructure to inter-individual variability in the ability to decode facial emotion expressions, and may explain why disruption of this pathway affects social behaviour.

Highlights

The Uncinate Fasciculus (UF) is a hook-shaped cortico-cortical white matter pathway that provides bidirectional connectivity between the orbital and medial prefrontal cortex (OMPFC), and the anterior portions of the temporal lobe (ATL), including the temporal pole, perirhinal cortex and amygdala (Petrides and Pandya, 2007; Schmahmann et al, 2007; Thiebaut de Schotten et al, 2012)
This suggests that the right UF may play an important role in the decoding of emotional content in facial expression, but be less critical to facial identity discrimination
To account for this procedural difference, Experiment 2 included a facial odd-emotion-out discrimination task that is more analogous to the odd-identity-out task used in Experiment 1

Summary

Introduction

The Uncinate Fasciculus (UF) is a hook-shaped cortico-cortical white matter pathway that provides bidirectional connectivity between the orbital and medial prefrontal cortex (OMPFC), and the anterior portions of the temporal lobe (ATL), including the temporal pole, perirhinal cortex and amygdala (Petrides and Pandya, 2007; Schmahmann et al, 2007; Thiebaut de Schotten et al, 2012). By virtue of its connectivity, the UF has been suggested to underpin a ‘temporo-amygdala-orbitofrontal network’ (Catani et al, 2013) or ‘anterior temporal system’ (Ranganath and Ritchey, 2012), potentially critical to the regulation of social and emotional behaviour (Von Der Heide et al, 2013), but the precise functions of this network are unspecified. We test the specific hypothesis that a critical role for the UF is in the decoding of facial expressions of emotion. Given that human social interactions are replete with emotional exchanges, facial emotion processing abilities are crucial for the regulation of interpersonal relationships and for social functioning more generally (Fischer and Manstead, 2008). Individual differences in the ability to decode facial expressions are linked

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