Altered Orbitofrontal Cortex Activation and Gaze Patterns to Happy Faces in Autistic Children Predict Adaptive Difficulties but Challenge the Social Motivation Hypothesis

Abstract

Individuals diagnosed with Autism Spectrum Disorder (ASD) generally have altered responses to social reward, which the “social motivation” hypothesis posits as the primary contributor to their social deficits. Aberrant perception of rewarding faces is considered to be one of the most significant markers of this hypothesis. The orbitofrontal cortex (OFC) plays an important role in modulating reward and arousal responses to happy faces but few studies have investigated whether young autistic children with limited cognitive or language ability have altered neural and behavioral responses to reward related tasks. We therefore conducted an eye-tracking task where autistic (n = 36) and typically developing (n = 36) young children (aged 2.5-6 years) viewed the faces of happy children or of simplified faces (emoticons), combined with OFC activation measurement using functional near infrared spectroscopy (fNIRS), to compare ASD and typically developing (TD) children. Results revealed no differences between the two groups for time spent viewing happy faces although TD children spent more time looking at the eyes of real faces and at the mouths of emoticons whereas children with ASD did not. Children with ASD showed a greater pupil diameter (PD) and OFC activation compared to TD children during presentation of happy faces. Indeed, greater PD and OFC responses were predictive of greater adaptive behavior difficulties and severity of symptoms. Our results therefore demonstrate different gaze patterns and greater arousal and brain reward system responses to happy faces in young children with ASD which are incongruent with social motivation hypothesis.Availability of dataOur ethics approval does not permit public archiving of individual anonymized raw data. Those who wish to access the raw data should contact the corresponding author. Access will be granted to named individuals who adhere to the ethical procedures governing the reuse of sensitive data. They must complete a formal data sharing agreement to obtain the data. The data that support the main group different finding figures related anonymized data of this study are openly available via the Open Science Framework (OSF) Repositoryhttps://osf.io/sxkhc/?view_only=6eb51e64a9b54fce909b5ff6eacdc668Ethics approval statementThe study was conducted in accordance with the principles of the Declaration of Helsinki. It was approved by the Local Ethics Committee (number 202165).Research Highlights●The present study examined whether altered social reward processing in ASD is caused by reduced behavioral and neural responses to rewarding stimuli.●Typically developing children showed a preference for viewing specific informative facial features (such as child eyes or emoticon mouths), children with autism did not.●Children with autism enhanced arousal (pupil dilation) and brain reward (orbitofrontal cortex) responses to happy child faces.●Altered, gaze patterns, arousal and brain reward responses were highly predictive of adaptive behavior abilities and autistic symptom severity.