Introduction: Humans possess the ability to reason and make inferences about another individual’s beliefs even when those beliefs differ from one’s own or are incongruent with the real state of the world. This capacity to maintain an updated, detailed model of another’s representation of the world is referred to as theory-of-mind and is thought to one of the most advanced features of human cognition. The single unit activity underlying this behavior is not known.
Methods: In patients undergoing awake surgery for deep brain stimulation implantation, we performed single unit recordings in the dorsal prefrontal cortex (dPFC)—an area previously shown to be involved in inferential processing1–3. We used a false-belief task in which participants were read 2-3 sentence vignettes describing a series of events between characters and were required to formulate ideas about the characters and their beliefs. To test for theory-of-mind activity we used linear discriminant analysis to compare neuronal decoding performance (prediction of true vs. false nature of vignette) when considering vignettes detailing modification in beliefs of others versus those detailing events in the absence of a social agent.
Results: We enrolled 11 participants and recorded from a total of 212 neurons. Decoding analysis revealed that many neurons reflected inferences made about other’s beliefs with a total of 49 (23.1%) showing differential firing rate when another’s beliefs were false vs. to true (as compared to participant’s own beliefs/understanding). Population decoding performance was highly predictive (74%) of another individual’s state of belief. Significantly decreased performance was observed for trials not containing social agents.
Conclusions: Taken together, these findings suggest a neuronal process involving dPFC neurons that enables humans to develop and maintain complex representations of others’ states of mind. Such computation may provide a framework for human theory-of-mind behavior and insight into how prefrontal cortical dysfunction may lead to cognitive and social impairment.
Patient Care: Theory-of-mind is critical to effective social interaction. Dysfunction of the neural computations involved in this behavior may underlie disorders that are characterized by impaired social interaction, including autism spectrum disorder. Therefore, understanding the neuronal basis for complex human cognitive and social behavior may provide a framework for understanding and treating such disorders in the future.
Learning Objectives: By conclusion of this session, participants should be able to (1) define theory-of-mind cognition, (2) explain the false-belief task and its role in assessing theory-of-mind behavior, and (3) describe dorsal prefrontal involvement in theory-of-mind computation.