What makes the dorsomedial frontal cortex active during reading the mental states of others?

Abstract

The dorsomedial frontal part of the cerebral cortex is consistently activated when people read the mental states of others, such as their beliefs, desires, and intentions, the ability known as having a theory of mind (ToM) or mentalizing. This ubiquitous finding has led many researchers to conclude that the dorsomedial frontal cortex (DMFC) constitutes a core component in mentalizing networks. Despite this, it remains unclear why the DMFC becomes active during ToM tasks. We argue that key psychological and behavioral aspects in mentalizing are closely associated with DMFC functions. These include executive inhibition, distinction between self and others, prediction under uncertainty, and perception of intentions, all of which are important for predicting others' intention and behavior. We review the literature supporting this claim, ranging in fields from developmental psychology to human neuroimaging and macaque electrophysiology. Because perceiving intentions in others' actions initiates mentalizing and forms the basis of virtually all types of social interaction, the fundamental issue in social neuroscience is to determine the aspects of physical entities that make an observer perceive that they are intentional beings and to clarify the neurobiological underpinnings of the perception of intentionality in others' actions.

Keywords: dorsomedial frontal cortex; executive function; intention; mentalizing; others; self; theory of mind; uncertainty.

Figure 1

Involvement of DMFC in executive inhibition. (A) When the animal successfully switched to a now-valid action by inhibiting a pre-potent, no-longer-valid action, pre-SMA “switch neurons” fired phasically before movement onset (red). Switching was unsuccessful when the initiation of activity increase was delayed (blue). (B) The contrast between inhibition vs. action trials revealed activation in the dorsal frontomedial cortex (BA 9). Reprinted with permission from Brass and Haggard (2007).

Figure 2

Involvement of DMFC in self-other distinction. A group of DMFC neurons (“partner-type neurons”) were preferentially activated when the recorded monkey observed another monkey making an action (blue), while another group of DMFC neurons (“self-type neurons”) were preferentially activated when the recorded monkey executed an action (red).

Figure 3

Involvement of DMFC in prediction under uncertainty. The contrast between prediction under uncertainty vs. control conditions revealed activation in several brain regions including the frontomedian cortex (BA 8). vST, ventral striatum; Tha, thalamus; VTA, midbrain area; Cu, cuneus; Ce, cerebellum. Reprinted with permission from Volz et al. (2003).

Figure 4

Involvement of DMFC in attention to and perception of intention. (A) Activation of the pre-SMA associated with attention to intention as compared to attention to movement. The time course of the hemodynamic response is shown on the right. Reprinted with permission from Lau et al. (2004). (B) Activation of BA 9 associated with anticipation of third-person actions as compared to non-biological agent (i.e., computer) actions. Reprinted with permission from Ramnani and Miall (2004). ^*P < 0.005. (one-tailed paired t-test).