Spatial relations and spatial locations are dissociated within prefrontal and parietal cortex

Abstract

Item-specific spatial information is essential for interacting with objects and for binding multiple features of an object together. Spatial relational information is necessary for implicit tasks such as recognizing objects or scenes from different views but also for explicit reasoning about space such as planning a route with a map and for other distinctively human traits such as tool construction. To better understand how the brain supports these two different kinds of information, we used functional MRI to directly contrast the neural encoding and maintenance of spatial relations with that for item locations in equivalent visual scenes. We found a double dissociation between the two: whereas item-specific processing implicates a frontoparietal attention network, including the superior frontal sulcus and intraparietal sulcus, relational processing preferentially recruits a cognitive control network, particularly lateral prefrontal cortex (PFC) and inferior parietal lobule. Moreover, pattern classification revealed that the actual meaning of the relation can be decoded within these same regions, most clearly in rostrolateral PFC, supporting a hierarchical, representational account of prefrontal organization.

Fig. 1.

Example trial sequences with correct responses shown for illustration. A: Item Horizontal trial; B: Item Vertical trial; C: Relation Horizontal trial; D: Relation Vertical trial. See materials and methods for details.

Fig. 2.

Univariate contrasts showing double dissociation between Items and Relations. A: Relations > Items, sample period. B: Items > Relations, delay period. R, right; L, left.

Fig. 3.

Searchlight weight maps for areas showing success in classification of Relation [voxels are hotter colors (red) to the extent that they “prefer” (i.e., were given positive weights by the support vector machine classifier) Relation trials] vs. Item [cooler colors (blue) to the extent that they prefer Items; negative weights] trials during sample (A) and delay (B) periods. Areas of intermediate shades (e.g., green) were those that either had a mix of large positive and negative weights, which were canceled out by smoothing, or had low weights for both conditions.

Fig. 4.

A and B: example weight maps generated by classifier for posterior parietal regions of interest (ROIs), showing an interdigitated pattern of voxel preferences for Relation (hotter colors) or Item (cooler colors) trials at the representative single-subject (A) and group (B) levels. C: classification results of Items vs. Relations within ROIs defined by significantly elevated activity in both Item and Relation trials and no trend toward differential activity between Item and Relation trials, showing that even within areas of common activation, dissociable neural subpopulations can by distinguished by their response patterns. Chance is 50%. BOCC, bilateral occipital cortex; LIPS, left intraparietal sulcus; BDOCC/PP, bilateral dorsal occipital/posterior parietal cortex; BFEF, bilateral frontal eye fields. *P < 0.05; †P < 0.005.

Fig. 5.

Areas in which information about item location could be decoded successfully via searchlight classification during sample (A) and delay (B) periods.

Fig. 6.

Successful searchlight classification of relations. A: classification of relational direction during delay. B and C: classification of relational magnitude in sample (B) and delay (C) periods.