Familiarity modulates mirror neuron and mentalizing regions during intention understanding

Abstract

Recent research suggests that the inference of others' intentions from their observed actions is supported by two neural systems that perform complementary roles. The human putative mirror neuron system (pMNS) is thought to support automatic motor simulations of observed actions, with increased activity for previously experienced actions, whereas the mentalizing system provides reflective, non-intuitive reasoning of others' perspectives, particularly in the absence of prior experience. In the current fMRI study, we show how motor familiarity with an action and perceptual familiarity with the race of an actor uniquely modulate these two systems. Chinese participants were asked to infer the intentions of actors performing symbolic gestures, an important form of non-verbal communication that has been shown to activate both mentalizing and mirror neuron regions. Stimuli were manipulated along two dimensions: (1) actor's race (Caucasian vs. Chinese actors) and (2) participants' level of experience with the gestures (familiar or unfamiliar). We found that observing all gestures compared to observing still images was associated with increased activity in key regions of both the pMNS and mentalizing systems. In addition, observations of one's same race generated greater activity in the posterior pMNS-related regions and the insula than observations of a different race. Surprisingly, however, familiar gestures more strongly activated regions associated with mentalizing, while unfamiliar gestures more strongly activated the posterior region of the pMNS, a finding that is contrary to prior literature and demonstrates the powerful modulatory effects of both motor and perceptual familiarity on pMNS and mentalizing regions when asked to infer the intentions of intransitive gestures.

Figure 1

Examples of still images of the stimuli. Participants observed 2‐s videos of familiar gestures (left panel), unfamiliar gestures (middle panel), and control still images (right panel). Each gesture and still image was performed by an actor of the participants' own race (Chinese) and an actor of a different race (Caucasian). Original videos were presented in full color.

Figure 2

Brain responses to observations of gestures versus still images (all images displayed at P < 0.001 uncorrected for visualization purposes; x = −51). A: Observation of all gestures across familiarity and races versus still images evoked greater activity in components of the pMNS [the left dorsal inferior frontal gyrus (IFG) and dorsal premotor cortex and inferior parietal lobule (IPL)], as well as the posterior superior temporal sulcus (pSTS) and posterior cingulate cortex (PCC; not shown). B: Observation of the same race versus still (red) evoked activity in the left IPL and pSTS, while observation of a different race versus still (green) evoked activity in the left dorsal premotor cortex and pSTS. C: Observation of familiar gestures versus still images (red) evoked greater activity in the left pSTS, while unfamiliar gestures versus still images (green) evoked activity in dorsal IFG, IPL, and pSTS.

Figure 3

Race‐driven and experience‐driven brain responses (all images displayed at P < 0.001 uncorrected for visualization purposes). A: Observations of another race versus one's own race (DifferentRace > SameRace) evoked greater activity in the occipital cortex bilaterally in the fusiform gyrus and middle temporal gyrus (area V5/MT; not shown; z = −11). B: Observations of one's own race versus another race (SameRace > DifferentRace) evoked greater activity in the left IPL and right posterior insula (not shown; x = −59). C: Observations of familiar gestures versus unfamiliar gestures (Familiar > Unfamiliar) evoked greater activity in the dorsal medial prefrontal cortex (dMPFC), the posterior cingulate (PCC), the cuneus, and the bilateral temporoparietal junctions (not shown), regions associated with mentalizing and reasoning processes (x = −4). D: Observations of unfamiliar gestures versus familiar gestures (Unfamiliar > Familiar) evoked greater activity in the left IPL and postcentral gyrus and the bilateral middle temporal gyri (area V5/MT) in the putative extrastriate body area (EBA; x = −53).