Disrupted Human–Dog Interbrain Neural Coupling in Autism-Associated Shank3 Mutant Dogs

Abstract

Dogs interact with humans effectively and intimately. However, the neural underpinnings for such interspecies social communication are not understood. It is known that interbrain activity coupling, i.e., the synchronization of neural activity between individuals, represents the neural basis of social interactions. Here, previously unknown cross-species interbrain activity coupling in interacting human–dog dyads is reported. By analyzing electroencephalography signals from both dogs and humans, it is found that mutual gaze and petting induce interbrain synchronization in the frontal and parietal regions of the human–dog dyads, respectively. The strength of the synchronization increases with growing familiarity of the human–dog dyad over five days, and the information flow analysis suggests that the human is the leader while the dog is the follower during human–dog interactions. Furthermore, dogs with Shank3 mutations, which represent a promising complementary animal model of autism spectrum disorders (ASD), show a loss of interbrain coupling and reduced attention during human–dog interactions. Such abnormalities are rescued by the psychedelic lysergic acid diethylamide (LSD). The results reveal previously unknown interbrain synchronizations within an interacting human–dog dyad which may underlie the interspecies communication, and suggest a potential of LSD for the amelioration of social impairment in patients with ASD.