Abstract

BackgroundImpaired social functioning is a common symptom of individuals with developmental disruptions in callosal connectivity. Among these developmental conditions, agenesis of the corpus callosum provides the most extreme and clearly identifiable example of callosal disconnection. To date, deficits in nonliteral language comprehension, humor, theory of mind, and social reasoning have been documented in agenesis of the corpus callosum. Here, we examined a basic social ability as yet not investigated in this population: recognition of facial emotion and its association with social gaze.MethodsNine individuals with callosal agenesis and nine matched controls completed four tasks involving emotional faces: emotion recognition from upright and inverted faces, gender recognition, and passive viewing. Eye-tracking data were collected concurrently on all four tasks and analyzed according to designated facial regions of interest.ResultsIndividuals with callosal agenesis exhibited impairments in recognizing emotions from upright faces, in particular lower accuracy for fear and anger, and these impairments were directly associated with diminished attention to the eye region. The callosal agenesis group exhibited greater consistency in emotion recognition across conditions (upright vs. inverted), with poorest performance for fear identification in both conditions. The callosal agenesis group also had atypical facial scanning (lower fractional dwell time in the eye region) during gender naming and passive viewing of faces, but they did not differ from controls on gender naming performance. The pattern of results did not differ when taking into account full-scale intelligence quotient or presence of autism spectrum symptoms.ConclusionsAgenesis of the corpus callosum results in a pattern of atypical facial scanning characterized by diminished attention to the eyes. This pattern suggests that reduced callosal connectivity may contribute to the development and maintenance of emotion processing deficits involving reduced attention to others' eyes.

Highlights

  • Impaired social functioning is a common symptom of individuals with developmental disruptions in callosal connectivity

  • Fullscale intelligence quotient (FSIQ) was correlated with accuracy of emotion recognition in the control group (7 emotions r = 0.76, p = 0.02, 95% confidence interval (CI) 0.20 to 0.95; 6 emotions f = 0.71, p = 0.03, 95% CI 0.08 to 0.93; Additional file 1: Table S1)

  • We found that adults with agenesis of the corpus callosum (AgCC) exhibit impairments in recognizing facial emotions and, that these impairments were directly associated with diminished gaze to the eye region in faces

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Summary

Introduction

Impaired social functioning is a common symptom of individuals with developmental disruptions in callosal connectivity. Deficits in nonliteral language comprehension, humor, theory of mind, and social reasoning have been documented in agenesis of the corpus callosum. There is evidence of poor comprehension of humor and nonliteral language forms due to a bias toward literal interpretation and difficulty using context to infer meaning [16,20,21] This impairment in making accurate second-order interpretations of linguistic information is a significant factor in the social profile of AgCC which includes poor conversation skills and restricted verbal expression of emotional experience (similar to alexithymia) [22,23], emotionally and logically impoverished verbal interpretation of social scenes [24,25], and impaired theory of mind in interpreting complex social interactions [26]

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