Intranasal oxytocin modulates brain responses to voice-identity recognition in typically developing individuals, but not in ASD

Abstract

Faces and voices are prominent cues for person-identity recognition. Face recognition behavior and associated brain responses can be enhanced by intranasal administration of oxytocin. It is unknown whether oxytocin can also augment voice-identity recognition mechanisms. To find it out is particularly relevant for individuals who have difficulties recognizing voice identity such as individuals diagnosed with autism spectrum disorder (ASD). We conducted a combined behavioral and functional magnetic resonance imaging (fMRI) study to investigate voiceidentity recognition following intranasal administration of oxytocin or placebo in a group of adults diagnosed with ASD (full-scale intelligence quotient > 85) and pairwise-matched typically developing (TD) controls. A single dose of 24 IU oxytocin was administered in a randomized, double-blind, placebo-controlled and cross-over design. In the control group, but not in the ASD group, administration of oxytocin compared to placebo increased responses to recognition of voice identity in contrast to speech in the right posterior superior temporal sulcus/gyrus (pSTS/G)a region implicated in the perceptual analysis of voice-identity information. In the ASD group, the right pSTS/G responses were positively correlated with voice-identity recognition accuracy in the oxytocin condition, but not in the placebo condition. Oxytocin did not improve voice-identity recognition performance at the group level. The ASD compared to the control group had lower right pSTS/G responses to voice-identity recognition. Since ASD is known to have atypical pSTS/G, the results indicate that the potential of intranasal oxytocin to enhance mechanisms for voice-identity recognition might be variable and dependent on the functional integrity of this brain region.

Oxytocin Dynamics in the Body and Brain Regulated by the Receptor for Advanced Glycation End-Products, CD38, CD157, and Nicotinamide Riboside

“…It has been established that OT is not only secreted from the posterior pituitary into the circulation but is also released in the brain, where it has very diverse behavioral effects ( Russell et al, 2003 ; Leng et al, 2015 ; Higashida, 2016 ; Russell, 2018 ). Hypothalamic neurons secrete oxytocin (OT) into the brain from dendrites and axons to function as an endogenous factor in species-specific social memory and behaviors, including emotion, interaction, and bonds ( Baumgartner et al, 2008 ; Bridges, 2015 ; Huang et al, 2015 ; Numan and Young, 2016 ; Feldman, 2017 ; Higashida et al, 2018 , 2019a , b ; Jurek and Neumann, 2018 ; Borowiak and von Kriegstein, 2020 ; Carter et al, 2020 ; Quintana and Guastella, 2020 ; Tolomeo et al, 2020 ; Froemke and Young, 2021 ; Grinevich and Neumann, 2021 ; Yeomans et al, 2021 ; Zheng and Kendrick, 2021 ; Carter, 2022 ). CD38 and CD157 play an essential role in central OT release ( Jin et al, 2007 ; Higashida et al, 2017b ).…”