fMRI reveals reciprocal inhibition between social and physical cognitive domains

Abstract

Two lines of evidence indicate that there exists a reciprocal inhibitory relationship between opposed brain networks. First, most attention-demanding cognitive tasks activate a stereotypical set of brain areas, known as the task-positive network and simultaneously deactivate a different set of brain regions, commonly referred to as the task negative or default mode network. Second, functional connectivity analyses show that these same opposed networks are anti-correlated in the resting state. We hypothesize that these reciprocally inhibitory effects reflect two incompatible cognitive modes, each of which may be directed towards understanding the external world. Thus, engaging one mode activates one set of regions and suppresses activity in the other. We test this hypothesis by identifying two types of problem-solving task which, on the basis of prior work, have been consistently associated with the task positive and task negative regions: tasks requiring social cognition, i.e., reasoning about the mental states of other persons, and tasks requiring physical cognition, i.e., reasoning about the causal/mechanical properties of inanimate objects. Social and mechanical reasoning tasks were presented to neurologically normal participants during fMRI. Each task type was presented using both text and video clips. Regardless of presentation modality, we observed clear evidence of reciprocal suppression: social tasks deactivated regions associated with mechanical reasoning and mechanical tasks deactivated regions associated with social reasoning. These findings are not explained by self-referential processes, task engagement, mental simulation, mental time travel or external vs. internal attention, all factors previously hypothesized to explain default mode network activity. Analyses of resting state data revealed a close match between the regions our tasks identified as reciprocally inhibitory and regions of maximal anti-correlation in the resting state. These results indicate the reciprocal inhibition is not attributable to constraints inherent in the tasks, but is neural in origin. Hence, there is a physiological constraint on our ability to simultaneously engage two distinct cognitive modes. Further work is needed to more precisely characterize these opposing cognitive domains.

Keywords: Anti-correlated networks; Default network; Dual-process theory; Task negative; Task-positive; fMRI.

Copyright © 2012 Elsevier Inc. All rights reserved.

Figures

Figure 1

Schematic illustration of task conditions

Figure 2

Timeline for tasks and resting trials

Figure 3

Brain areas sensitive to cognitive domain and antagonistic areas. Colored areas pass multiple comparison correction in both video and text conditions independently. Warm colors (pink, red, orange, yellow) activate more for social than mechanical reasoning. Cool colors (purple, blue, cyan, green) activate more for mechanical than social reasoning. Bright colors (orange, yellow, cyan, green) identify antagonistic areas, which are significantly above rest for both tasks in one domain, and significantly below rest for both tasks in the other domain. Contrasts in each domain are cumulative, i.e. mechanical areas in blue have passed the contrast for purple (Physics>Social, fixed), areas in cyan have passed for purple and blue, and areas in green have passed for purple, blue and cyan. Graphs A-F show timecourses from antagonistic areas, without correction for hemodynamic lag. Blue and green shading indicate time points associated with stimulus and response periods, respectively. Error bars show standard error of mean across participants.

Figure 4

Correspondence between antagonistic areas derived using task induced deviations from rest and anti-correlations networks derived from resting functional connectivity (without regressing whole brain signal). All areas corrected for multiple comparisons. Resting connectivity data from a separate group of subjects was used to derive regions anti-correlated with social antagonistic areas, and separately with mechanical antagonistic areas. The overlap of these anti-correlated areas with antagonistic areas is shown. Core brain areas involved in social reasoning tend to suppress core regions involved in mechanical reasoning, and vice-versa, even during unconstrained thought in the absence of a task.

Figure 5

Influence of text length and task difficulty on average activity in the social and mechanical networks (defined by random effects strict conjunction). Voxelwise analyses failed to identify any significant differences in individual regions due to these potential confounds (see section 3.4).

Figure 6

Influence of Question valence (correct answer yes or no) and response accuracy on average activity in the social and mechanical networks (defined by random effects strict conjunction). Voxelwise analyses failed to identify any significant differences in individual regions due to these potential confounds (see section 3.4).

Figure 7

Comparison of default-mode regions associated with internal attention and/or spontaneous cognition, and default-mode regions associated with the division between social vs mechanical reasoning. The default-mode network is shown in green. (A) Regions that are more active during rest than any of the four tasks used here are shown in blue. Overlap between default-mode network and consistently deactivated areas shown in light green and blue. (B) Regions preferring Social to mechanical reasoning are shown in red. Overlap with default-mode network shown in yellow/light green.

Figure 8

Three cognitive stances, their relationships to each other, and the brain networks involved. Bidirectional arrows indicate mutual compatibility; barbell indicates mutual antagonism. The Intentional stance is a distinct cognitive mode in which processes associated with the task positive network operate on representations stored in the default network. Nonetheless, there remains a fundamental tension between cognitive modes involved in the representation of experiential mental states (the Phenomenal stance) and the representation of physical mechanisms (the Physical stance). The opposing domains hypothesis holds that this tension represents the cognitive basis of the reciprocal inhibition between default and task positive networks.