Heightened gaze responsiveness and mutual gaze instability at close distances characterize dyadic coordination in a marmoset model of autism

Autism spectrum disorder (ASD) is associated with differences in social interaction, including alterations in gaze behavior and interpersonal distance. Although most assessments of ASD remain individual-centric, emerging human studies indicate that social difficulties may arise from atypical dyadic coordination rather than from reduced social interest alone. We examined dyadic coordination in a non-human primate model of ASD, focusing on gaze and inter-individual distance during minimally constrained first encounters between prenatal valproic acid-exposed marmosets (VPA) and unexposed conspecifics (UE).

Markerless pose estimation quantified frame-by-frame gaze direction and spacing, comparing VPA–UE with UE–UE dyads. VPA–UE pairs exhibited a higher proportion of mutual-gaze events than UE–UE pairs. VPA individuals showed more rapid looks in response to the partner’s gaze, yet exhibited a lower proportion of one-sided looking events.

VPA–UE dyads maintained shorter inter-individual distances than UE–UE dyads, and closer spacing was associated with decreased stability of mutual gaze. These findings reveal a dyadic coordination pattern in VPA–UE pairs, with rapid responsiveness coupled with a distance-dependent reduction in time spent in mutual gaze, paralleling features reported in human ASD. Our dyad-centric, markerless framework yields ecologically grounded readouts and potential intervention targets that leverage intact social responsiveness while accommodating altered spatial coordination.

Atsushi Senjyu from Hamamatsu University School of Medicine for constructive feedback. Kazuhiko Yamaguchi from NCNP for their helpful discussions. Naomi Hasegawa, Akiko Tsuchiya, Ryoichi Saito, and other members of the NCNP primate facility for their invaluable support with experiments and animal care.

Finally, we extend special thanks to all the subject marmosets. This work was supported by the Intramural Research Grant for Neurological and Psychiatric Disorders of the National Center of Neurology and Psychiatry (Grant No. 2–7 to N.I.), the Japan Agency for Medical Research and Development (AMED) (Grant No. 25wm0625206h0002 to N.I., Grant No. 25wm0625124h0002 to K.M.), JST CRONOS (Grant No. JPMJCS24K7 to Tsuyoshi S.) and KAKENHI (Grant No. 21H04421 to N.

United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo, Japan Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo, Japan Madoka Nakamura, Tomoko Sato, Tohru Kurotani, Kazuhisa Sakai & Noritaka Ichinohe Department of Mental Disorder Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo, Japan Department of Cognitive and Psychological Sciences, Graduate School of Informatics, Nagoya University, Aichi, Japan Academy of Emerging Sciences, Chubu University, Aichi, Japan Correspondence to Tsuyoshi Shimmura or Noritaka Ichinohe. The authors declare no competing interests. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.