Brain system for mental orientation in space, time, and person

Abstract

Orientation is a fundamental mental function that processes the relations between the behaving self to space (places), time (events), and person (people). Behavioral and neuroimaging studies have hinted at interrelations between processing of these three domains. To unravel the neurocognitive basis of orientation, we used high-resolution 7T functional MRI as 16 subjects compared their subjective distance to different places, events, or people. Analysis at the individual-subject level revealed cortical activation related to orientation in space, time, and person in a precisely localized set of structures in the precuneus, inferior parietal, and medial frontal cortex. Comparison of orientation domains revealed a consistent order of cortical activity inside the precuneus and inferior parietal lobes, with space orientation activating posterior regions, followed anteriorly by person and then time. Core regions at the precuneus and inferior parietal lobe were activated for multiple orientation domains, suggesting also common processing for orientation across domains. The medial prefrontal cortex showed a posterior activation for time and anterior for person. Finally, the default-mode network, identified in a separate resting-state scan, was active for all orientation domains and overlapped mostly with person-orientation regions. These findings suggest that mental orientation in space, time, and person is managed by a specific brain system with a highly ordered internal organization, closely related to the default-mode network.

Keywords: cognitive map; default network; disorientation; fMRI; precuneus.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Midsagittal cortical activity during orientation in space, time, and person. (A) Domain-specific activity in a representative subject, identified by contrasting activity between each orientation domain and the other two domains. The precuneus region is active in all three orientation domains, and the medial prefrontal cortex only in person and time orientation (P < 0.05, FDR-corrected, cluster size >20 voxels). Dashed black lines represent the limit of the scanned region in this subject. (B) Precuneus activity in four subjects, demonstrating a highly consistent posterior–anterior organization (white dashed line); all other subjects showed the same activity pattern (Fig. S1). (C) Group average (n = 16) of event-related activity in independent experimental runs demonstrates the specificity of each cluster to one orientation domain. Lines represent activity in response to space (blue), time (green), and person (red) conditions. Error bars represent SEM between subjects. (D) Group average of beta plots from volume-of-interest GLM analysis, showing highly significant domain-specific activity. Error bars represent SEM between subjects. P, person; S, space; T, time.

Fig. 2.

Lateral cortical activity during orientation in space, time, and person. (A) Domain-specific activity in a representative subject, identified by contrasting activity between each orientation domain and the other two domains (P < 0.05, FDR-corrected, cluster size >20 voxels). The inferior parietal lobe (IPL) is active in all three orientation domains, and the temporal lobe mostly for time but also for person orientation. Notice the strong left lateralization of time activations. (B) IPL activity in four subjects, demonstrating a consistent posterior–anterior organization (white dashed line): All other subjects showed the same activity pattern (Fig. S1). (C) Group average (n = 16) event-related plots from independent experimental runs. (D) Group average of beta plots from volume-of-interest GLM analysis. See Fig. 1 legend for further details.

Fig. S1.

Cortical activity during orientation in space, time, and person in individual subjects. Domain-specific activity is shown for all 16 subjects, obtained by contrasting activity between each orientation domain and the other two domains (P < 0.05, FDR-corrected, cluster size >20 voxels). Dashed lines represent the limit of the scanned region in each subject. Subject 13 could not be transformed to an inflated brain representation due to technical reasons and is therefore presented by representative slices. Notice the consistent pattern of activity in the inferior parietal, medial parietal, frontal and temporal cortices.

Fig. S2.

Overlap between activations in the different orientation domains in individual subjects. Overlapping and nonoverlapping activity is shown for all 16 subjects, obtained by contrasting activity between each orientation domain (space, time, and person) and a lexical control task (P < 0.05, FDR-corrected, cluster size >20 voxels). Significant overlap was found in 14/16 subjects. Subject 13 could not be transformed to an inflated brain representation due to technical reasons.

Fig. S3.

Random-effects group analysis. All 16 subjects were analyzed with a random-effects group analysis. (A) Contrast between each orientation domain (space, time, or person) and the other two domains, indicating regions of domain-specific activity (P < 0.05, FDR-corrected, cluster size >20 voxels). (B) Contrast between each orientation domain and the lexical control task (P < 0.05, FDR-corrected, cluster size >20 voxels). Dashed lines indicate borders of regions scanned in all 16 subjects, on which the analysis was performed. The Venn diagram (bottom right) demonstrates the prominent overlap between activations in the precuneus and inferior parietal regions.

Fig. S4.

Probabilistic-maps group analysis. Two groups of subjects were analyzed separately based on the coverage of their functional scans: 10 subjects scanned with frontal and parietal coverage (Left), and 6 subjects scanned with temporal and parietal coverage (Right). (A) Contrast between each orientation domain (space, time, or person) and the other two domains, indicating regions of domain-specific activity. (B) Contrast between each orientation domain and the lexical control task. Original maps used for group analysis are presented in Figs. S1 and S2 and are FDR-corrected and cluster size-thresholded at 20 voxels per cluster. The probabilistic maps presented here are thresholded at 25% of subjects of each group.

Fig. 3.

Overlap between activations in the space, time, and person domains. (A) Overall orientation-related activity in a representative subject, identified by contrasting activity between each orientation domain and the lexical control task, showing overlap between regions (P < 0.05, FDR-corrected, cluster size >20 voxels). (B) Group average of the percent of overlap between active voxels in each orientation domain, demonstrating a partial overlap between domains (for group-level results, see Figs. S3B and S4B).

Fig. 4.

Overlap of orientation activity with the default mode network (DMN). The DMN was identified using resting-state fMRI in each individual subject. The DMN is presented for a representative subject, overlaid with activity during the orientation task in space, time, and person (identified by contrasting activity between each orientation domain and the other two domains). (A) Midsagittal view, focus on the precuneus. (B) Lateral view, focus on the IPL. (C) Average percent, across subjects, of DMN voxels from all voxels active specifically for a single orientation domain. DMN voxels were found most prominently in the person domain (two-tailed t test, all P < 0.01) although some were found also in the time and space domains. P, person; S, space; T, time.

Fig. S5.

Overlap between the default-mode network (DMN) and activity during orientation in the person domain for individual subjects. An ICA component clearly corresponding to the DMN could be identified in 13 out of the 16 subjects. A clear overlap is apparent between the DMN and regions of person orientation.

Fig. S6.

Overlap between the default-mode network (DMN) and activity during orientation in the space domain for individual subjects. Regions of spatial orientation generally lie outside and adjacent to the default-mode network although some overlap exists.

Fig. S7.

Overlap between the default-mode network (DMN) and activity during orientation in the time domain for individual subjects. Regions of temporal orientation generally lie outside and adjacent to the default-mode network, although some overlap exists. Notice also the strong left-lateralization of time activations.

Fig. S8.

Average DMN overlap with orientation domains for individual subjects. In each brain region, the average overlap of DMN with each domain-specific region (contrast between each orientation domain and the other two domains) is calculated as the number of DMN voxels in each domain divided by the total number of DMN voxels.

Fig. S9.

Event-related time courses from default-mode networks nodes, for the different orientation domains. The default-mode network is similarly active across all orientation domains in the precuneus and inferior parietal lobes, and only for the person domain in the medial prefrontal lobe (blue, space; red, person; green, time; error bars represent SEM between subjects).