Where is the "where" in the brain? A meta-analysis of neuroimaging studies on spatial cognition

Abstract

Spatial representations are processed in the service of several different cognitive functions. The present study capitalizes on the Activation Likelihood Estimation (ALE) method of meta-analysis to identify: (a) the shared neural activations among spatial functions to reveal the "core" network of spatial processing; (b) the specific neural activations associated with each of these functions. Following PRISMA guidelines, a total of 133 fMRI and PET studies were included in the meta-analysis. The overall analysis showed that the core network of spatial processing comprises regions that are symmetrically distributed on both hemispheres and that include dorsal frontoparietal regions, presupplementary motor area, anterior insula, and frontal operculum. The specific analyses revealed the brain regions that are selectively recruited for each spatial function, such as the right temporoparietal junction for shift of spatial attention, the right parahippocampal gyrus, and the retrosplenial cortex for navigation and spatial long-term memory. The findings are integrated within a systematic review of the neuroimaging literature and a new neurocognitive model of spatial cognition is proposed.

Keywords: activation likelihood estimation; frontoparietal; long-term memory; mental rotation; meta-analysis; navigation; neuroimaging; spatial attention; spatial cognition; spatial working memory.

Figure 1

Core network for spatial processing. The figure represents the results of the meta‐analysis including all the eligible studies (a) and the results of the meta‐analysis including only the studies that applied the correction for multiple comparisons to their results (b); in the third panel (c), the overlap between the two meta‐analyses is graphically represented

Figure 2

Spatial attention related activations. The figure represents the 2D (a) and 3D (b) brain activations during attention tasks. In the C panel, the selective activations for attention (attention—Working memory+navigation+mental rotation) are represented [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Spatial working memory related activations. The figure represents the 2D (a) and 3D (b) brain activations during working memory tasks. In the (c) panel, the selective activations for working memory (working memory—Attention+navigation+mental rotation) are represented [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Spatial long‐term memory and navigation related activations. The figure represents the 2D (a) and 3D (b) brain activations during long‐term memory and navigation tasks. In the (c) panel, the selective activations for long‐term memory and navigation (LTM + navigation—Mental rotation+navigation+working memory) are represented [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Mental rotation and spatial imagery related activations. The figure represents the 2D (a) and 3D (b) brain activations during mental rotation and spatial imagery tasks. In the (c) panel, the selective activations for these processes (mental rotation+spatial imagery—Attention+navigation+working memory) are represented [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 6

Schematic model of spatial processing. This figure represents a schematic illustration of the proposed model for spatial processing. Spatial inputs processed in visual regions lead to a shift of attention, mediated by the right ventral frontoparietal network, comprising TPJ and inferior frontal gyrus. Dorsal frontal and superior parietal lobe regions, forming the dorsal attention network (DAN), are then activated and serve to allocate internal attention toward the spatial representations to keep them active. The pre‐SMA acts in cooperation with the DAN and is responsible to integrate sequential spatial information into a coherent map of space. Such maps of space are then prioritized by frontal operculum and the insular cortex based on both the individuals' goals and the external stimuli. Posterior parahippocampal and retrosplenial regions are instead recruited selectively in long‐term memory processes, such as spatial maps storage and recognition of landmarks. Pre‐SMA, presupplementary motor area; SPL, superior parietal lobe; TPJ, temporoparietal junction [Color figure can be viewed at http://wileyonlinelibrary.com]