Distinct regions of medial rostral prefrontal cortex supporting social and nonsocial functions

Abstract

While some recent neuroimaging studies have implicated medial rostral prefrontal cortex (MPFC) in 'mentalizing' and self-reflection, others have implicated this region in attention towards perceptual vs self-generated information. In order to reconcile these seemingly contradictory findings, we used fMRI to investigate MPFC activity related to these two functions in a factorial design. Participants performed two separate tasks, each of which alternated between 'stimulus-oriented phases' (SO), where participants attended to task-relevant perceptual information, and 'stimulus-independent phases' (SI), where participants performed the same tasks in the absence of such information. In half of the blocks ('mentalizing condition'), participants were instructed that they were performing these tasks in collaboration with an experimenter; in other blocks ('non-mentalizing condition'), participants were instructed that the experimenter was not involved. In fact, the tasks were identical in these conditions. Neuroimaging data revealed adjacent but clearly distinct regions of activation within MPFC related to (i) mentalizing vs non-mentalizing conditions (relatively caudal/superior) and (ii) SO vs SI attention (relatively rostral/inferior). These results generalized from one task to the other, suggesting a new axis of functional organization within MPFC.

Fig. 1

Schematic illustration of the two behavioral tasks. In the ‘spatial’ task (SO phase), participants repeatedly pressed one of two response buttons, as if navigating around the edge of a complex shape in a clockwise direction, to indicate whether the next corner would require a left or a right turn. During the SI phase this shape was replaced by a ‘thought-bubble’ shape and participants were required to imagine the shape that was presented in the SO phase and continue navigating as before. In the ‘alphabet’ task (SO phase), participants classified upper-case letters of the alphabet according to whether they were composed of straight lines or curves. The stimuli cycled through the alphabet, skipping two letters between each stimulus and the next. In the SI phase the letters were replaced with question marks. Participants mentally continued the sequence and continued classifying letters as before.

Fig. 2

Panel A: functional subdivision of rostral PFC according to an earlier meta-analysis of functional neuroimaging studies (Gilbert et al., , adapted from Figure 6). Panel B: regions of activation in the present study for contrasts related to attention (SO > SI, shown in green) and mentalizing (mentalizing > non-mentalizing, shown in red), thresholded at P < 0.001 uncorrected. Results are displayed on axial slices (z = 24) of the participants’ mean normalized structural image.

Fig. 3

Regions of activation related to attention (SO > SI, shown in green), mentalizing (mentalizing > non-mentalizing, shown in red), and their overlap (blue). Contrasts were thresholded at P < 0.001 uncorrected and plotted on the participants’ mean normalized structural image.

Fig. 4

BOLD signal associated with the four experimental conditions, in each task. Left panel: results from the peak MPFC region identified in the contrast of SO > SI. Right panel: results from the peak MPFC region identified in the contrast of mentalizing > non-mentalizing. Results indicate the mean parameter estimate in each condition from a 6 mm-radius sphere centered on the relevant activation peak. All results are plotted relative to the stimulus-expectation condition, i.e. the period at the beginning of each block before any stimulus is presented. Error bars represent standard errors.

Fig. 5

Mean peak y (left panel) and z (right panel) co-ordinates within BA 10 for the contrasts related to attention (SO > SI) and mentalizing (mentalizing > non-mentalizing), at each sagittal slice between x = −8 and x = +8. Error bars represent standard errors.