Single-neuronal predictions of others’ beliefs in humans

Abstract

Human social behavior crucially depends on our ability to reason about others. This capacity for ‘theory of mind’ plays a vital role in social cognition because it allows us not only to form a detailed understanding of the hidden thoughts and beliefs of other individuals but to also understand that they may differ from our own 1 – 3 . Although a number of areas in the human brain have been linked to social reasoning 4 , 5 and its disruption across a variety of psychosocial disorders 6 – 8 , the basic cellular mechanisms that underlie human theory of mind remain undefined. Using a rare opportunity to acutely record from single cells in the human dorsomedial prefrontal cortex, we discover neurons that reliably encode information about others’ beliefs across richly varying scenarios and that distinguish self- from other-belief related representations. By further following their encoding dynamics, we show how these cells represent the contents of the other’s beliefs and accurately predict whether they are true or false. We also show how they track inferred beliefs from another’s specific perspective and how their activities relate to behavioral performance. Together, these findings reveal a detailed cellular process in the human dorsomedial prefrontal cortex for representing another’s beliefs and identify candidate neurons that could support theory of mind.

Substrates of Human Prediction Error for Incentives, Perception, Cognition, and Action

“…We did, however, find greater responses to social than non-social PE in the dmPFC (Fig. 7C), consistent with the engagement of this region during theory of mind tasks measured with functional imaging 84 and single unit recording 30 . It is possible that this region represents PEs specific to the social domain, although this was not clearly the case at the single neuron level 30 .…”

“…7C), consistent with the engagement of this region during theory of mind tasks measured with functional imaging 84 and single unit recording 30 . It is possible that this region represents PEs specific to the social domain, although this was not clearly the case at the single neuron level 30 . Some theories of cognitive function and dysfunction posit domainspecific mechanisms 85 .…”

“…We also found relatively more activation for social PEs than other reward PEs in the ventral striatum, subgenual cingulate, dmPFC, claustrum, parietal lobe, and ventromedial and orbitofrontal PFC (Figure 7C). Notably, these regions are not unique to social processes or to social PEs 28,29 , although recent single-unit recordings in human dmPFC during performance of a 'theory of mind' task did show selectivity for prediction errors about others' beliefs, there were neurons that were selective for sensory PEs and neurons sensitive both to violations of others' belief states and sensory states too 30 . In our analyses, a contrast comparing reward PEs to social PEs showed regions including dorsal and ventral striatum, anterior and posterior cingulate, orbitofrontal cortex, thalamus, supplementary motor area, parietal lobe, midbrain, and parahippocampal gyrus were more engaged for reward PE.…”

Natural language syntax complies with the free-energy principle

“…Lastly, and pertaining more directly to existing work on active inference and linguistic communication (e.g., Vasil et al 2020), it is also notable that the recursive combinatorial apparatus of natural language syntax has been argued to facilitate recursive theory of mind ('I know that you know that Mary thinks that …') (Arslan et al 2017, Jamali et al 2021, and as such could in turn be seen as deriving some active inference-based properties of higher-order cognition, unveiling the latent or hidden states that are other people's mental states. Epistemic foraging aims to reduce uncertainty about the environment, and this is precisely what syntactic phrases do (Hippisley 2015).…”

Large-scale neural recordings with single-cell resolution in human cortex using high-density Neuropixels probes

“…Two separate stabilization approaches were tested. One approach involved the patients receiving DBS implantations at MGH, who normally also undergo standardized micro-electrode recording to optimize anatomical targeting 1,14 , Neuropixels probes were inserted in the same locations as the microelectrodes that traverse the dorsal lateral surface of the prefrontal cortex on the way to the target nucleus, offering a brief chance to study neuronal dynamics in the dlPFC and not perturbing the planned operative approach nor alter clinical care 1–3,14–16 . Three cannulae were placed in a manipulator (AlphaOmega Engineering, Nazareth, Israel) and the Neuropixels probe was attached to the cannulae using SteriStrips (3M™ Steri-Strip™ Reinforced Adhesive Skin Closures).…”