Macaques Exhibit Implicit Gaze Bias Anticipating Others’ False-Belief-Driven Actions via Medial Prefrontal Cortex

• Published in: Cell reports (Cambridge) 2020-03, Vol.30 (13), p.4433-4444.e5
• Main Authors: Hayashi, Taketsugu, Akikawa, Ryota, Kawasaki, Keisuke, Egawa, Jun, Minamimoto, Takafumi, Kobayashi, Kazuto, Kato, Shigeki, Hori, Yukiko, Nagai, Yuji, Iijima, Atsuhiko, Someya, Toshiyuki, Hasegawa, Isao
• Format: Article
• Language: English
• Subjects: Analysis of Variance; Animals; anticipatory-looking; Behavior, Animal; chemogenetic silencing; Culture; DREADDs; false belief; Female; Fixation, Ocular - physiology; gaze bias; hM4Di; Macaca; macaque; Male; medial prefrontal cortex; Neurons - physiology; non-human primate; Prefrontal Cortex - physiology; theory of mind
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.03.013

The ability to infer others’ mental states is essential to social interactions. This ability, critically evaluated by testing whether one attributes false beliefs (FBs) to others, has been considered to be uniquely hominid and to accompany the activation of a distributed brain network. We challenge the taxon specificity of this ability and identify the causal brain locus by introducing an anticipatory-looking FB paradigm combined with chemogenetic neuronal manipulation in macaque monkeys. We find spontaneous gaze bias of macaques implicitly anticipating others’ FB-driven actions. Silencing of the medial prefrontal neuronal activity with inhibitory designer receptor exclusively activated by designer drugs (DREADDs) specifically eliminates the implicit gaze bias while leaving the animals’ visually guided and memory-guided tracking abilities intact. Thus, neuronal activity in the medial prefrontal cortex could have a causal role in FB-attribution-like behaviors in the primate lineage, emphasizing the importance of probing the neuronal mechanisms underlying theory of mind with relevant macaque animal models. [Display omitted] •Macaques exhibit implicit gaze bias anticipating others’ false-belief-driven actions•Inhibitory DREADDs silencing medial prefrontal neurons abolish the gaze bias•Macaques and humans share brain networks for false-belief attribution-like behaviors•Among the network, the medial prefrontal cortex is causally linked to mental attribution Hayashi et al. ask whether only hominids possess theory of mind. They show macaques’ implicit gaze bias anticipating others’ false-belief-guided actions, which is abolished by chemogenetic silencing of the medial prefrontal cortex. Thus, false-belief attribution-like behaviors of non-human primates are underpinned by shared neuronal mechanisms with humans.