Ventral-Dorsal Functional Contribution of the Posterior Cingulate Cortex in Human Spatial Orientation: A Meta-Analysis

Abstract

The retrosplenial cortex has long been implicated in human spatial orientation and navigation. However, neural activity peaks labeled "retrosplenial cortex" in human neuroimaging studies investigating spatial orientation often lie significantly outside of the retrosplenial cortex proper. This has led to a large and anatomically heterogenous region being ascribed numerous roles in spatial orientation and navigation. Here, we performed a meta-analysis of functional Magnetic Resonance Imaging (fMRI) investigations of spatial orientation and navigation and have identified a ventral-dorsal functional specialization within the posterior cingulate for spatial encoding vs. spatial recall. Generally, ventral portions of the posterior cingulate cortex were more likely to be activated by spatial encoding, i.e., passive viewing of scenes or active navigation without a demand to respond, perform a spatial computation, or localize oneself in the environment. Conversely, dorsal portions of the posterior cingulate cortex were more likely to be activated by cognitive demands to recall spatial information or to produce judgments of distance or direction to non-visible locations or landmarks. The greatly varying resting-state functional connectivity profiles of the ventral (centroids at MNI -22, -60, 6 and 20, -56, 6) and dorsal (centroid at MNI 4, -60, 28) posterior cingulate regions identified in the meta-analysis supported the conclusion that these regions, which would commonly be labeled as "retrosplenial cortex," should be more appropriately referred to as distinct subregions of the posterior cingulate cortex. We suggest that future studies investigating the role of the retrosplenial and posterior cingulate cortex in spatial tasks carefully localize activity in the context of these identifiable subregions.

Keywords: cognitive map; hippocampus; navigation; retrosplenial; spatial memory.

Figure 1

Brodmann’s original depiction of the retrosplenial cortex (A), which was intentionally overrepresented (Brodmann, 2006). More modern illustrations based off the work by Morris et al. (2000) and Vogt et al. (2001) in panels (B,C), respectively, depict a substantially humbler region. Brodmann’s figures, originally published in 1910, are in the public domain.

Figure 2

Panel (A) depicts the frequency at which a coordinate label included “Retrosplenial Cortex” appeared within 2 mm of any given MNI Y, Z position, projected onto an MNI standard brain at x = 8 mm. Panel (B) depicts the volume of interest generated to encompass the brain tissue commonly referred to as “retrosplenial cortex” in the spatial cognition literature.

Figure 3

Multilevel kernel density analysis (MKDA) results depicting regions more likely to be activated by spatial encoding (red/yellow) and spatial recall (blue/green). Panels (A–C) are displayed at MNI 8, −53, 5, color range bounds represent uncorrected thresholds of p < 0.01 at t₍₄₄₎ = 2.69 and p < 0.001 at t₍₄₄₎ = 3.50 in an 8385-voxel region of interest (Figure 2B). Panel (D) displays a volumetric depiction of the significant clusters at p < 0.001.

Figure 4

Panel (A) depicts the difference in functional connectivity between the ventro-lateral posterior cingulate seeds more associated with spatial encoding, and the dorso-medial posterior cingulate seed more associated with spatial recall. Highlighted regions display significantly different functional connectivity profiles at p_fdr < 0.001. N = 38. Panel (B) displays grouped histograms of the differences in functional connectivity; red highlighting for more positive functional connectivity with the spatial encoding seeds, and blue for more positive functional connectivity with the spatial recall seed.