Abstract
Intranasal administration of the neuropeptide oxytocin (IN-OT) is increasingly considered as a potential treatment for targeting the core symptoms of autism spectrum disorder (ASD), but the effects of continual use on neural substrates are fairly unexplored and long-term effects are unknown. In this double-blind, randomized, placebo-controlled study, we investigated the effects of single-dose and multiple-dose IN-OT treatment (4 weeks of daily (24 IU) administrations) on brain activity related to processing emotional states. Thirty-eight adult men with ASD (aged between 18 and 35 years) underwent functional magnetic resonance imaging of the posterior superior temporal gyrus (pSTS) and amygdala regions while processing emotional states from point-light biological motion. In line with prior research, a single dose of IN-OT induced a reliable increase in pSTS brain activity during the processing of point-light biological motion, but no consistent long-term changes in pSTS activity were induced after the multiple-dose treatment. In terms of bilateral amygdala, the multiple-dose treatment induced a consistent attenuation in brain activity, which outlasted the period of actual administrations until four weeks and one year post-treatment. Critically, participants with stronger attenuations in amygdala-activity showed greater behavioral improvements, particularly in terms of self-reported feelings of avoidant attachment and social functioning. Together, these observations provide initial insights into the long-lasting neural consequences of chronic IN-OT use on amygdala functioning and provide first indications that the acute versus chronic effects of IN-OT administration may be qualitatively different. Larger studies are however warranted to further elucidate the long-term impact of IN-OT treatment on human neural substrates and its behavioral consequences.
Highlights
Intranasal administration of the neuropeptide oxytocin (IN-OT) is increasingly explored as a potential pharmacotherapy for targeting the core symptoms of autism spectrum disorder (ASD), a prevalent neurodevelopmental disorder characterized by impairments in social and communicative functioning and stereotyped and repetitive behavior
In the current study, we investigated the effects of single-dose and multiple-dose IN-OT treatment on neural activation during the processing of emotional states from point-light biological motion in adult men with ASD
In terms of neural activity at the level of the posterior superior temporal gyrus (pSTS), we mainly identified an acute effect of IN-OT (30 min after single-dose administration), indicating an increase in pSTS activity in the IN-OT, compared to the PL group
Summary
Intranasal administration of the neuropeptide oxytocin (IN-OT) is increasingly explored as a potential pharmacotherapy for targeting the core symptoms of autism spectrum disorder (ASD), a prevalent neurodevelopmental disorder characterized by impairments in social and communicative functioning and stereotyped and repetitive behavior. Initial single-dose administration studies in ASD have consistently demonstrated behavioral improvements on various social tasks[4,5,6,7,8] 22) and individuals with ASD5,23–28 provided evidence that singledose IN-OT administration can alter activations in brain regions involved in socio-communicative processing and salience networks, by modulating attention to and perception of biologically relevant stimuli, such as social information conveyed by eyes, faces, or biological motion[20]. Previous IN-OT administration studies have demonstrated improved biological motion perception[29,30,31] and increased activity in the posterior superior temporal sulcus (pSTS)—a core brain region involved in socio-communicative processing[23]
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