The neural basis for spatial relations

Abstract

Studies in semantics traditionally focus on knowledge of objects. By contrast, less is known about how objects relate to each other. In an fMRI study, we tested the hypothesis that the neural processing of categorical spatial relations between objects is distinct from the processing of the identity of objects. Attending to the categorical spatial relations compared with attending to the identity of objects resulted in greater activity in superior and inferior parietal cortices (especially on the left) and posterior middle frontal cortices bilaterally. In an accompanying lesion study, we tested the hypothesis that comparable areas would be necessary to represent categorical spatial relations and that the hemispheres differ in their biases to process categorical or coordinate spatial relations. Voxel-based lesion symptom mapping results were consistent with the fMRI observations. Damage to a network comprising left inferior frontal, supramarginal, and angular gyri resulted in behavioral impairment on categorical spatial judgments. Homologous right brain damage also produced such deficits, albeit less severely. The reverse pattern was observed for coordinate spatial processing. Right brain damage to the middle temporal gyrus produced more severe deficits than left hemisphere damage. Additional analyses suggested that some areas process both kinds of spatial relations conjointly and others distinctly. The left angular and inferior frontal gyrus processes coordinate spatial information over and above the categorical processing. The anterior superior temporal gyrus appears to process categorical spatial information uniquely. No areas within the right hemisphere processed categorical spatial information uniquely. Taken together, these findings suggest that the functional neuroanatomy of categorical and coordinate processing is more nuanced than implied by a simple hemispheric dichotomy.

Figure 1

Examples of the sequence of stimuli used in the fMRI study, (A) spatial condition and (B) object condition. Images labeled for purposes of this figure; images used in the scanner were unlabeled and in color. The arrow indicated the figure object in the spatial relations condition.

Figure 2

(A–G) Averaged time series for ROIs displaying significant differences between conditions. Time series were averaged across all blocks for each subject and then across all subjects for each experiment. Solid line depicts the average; dotted lines depict average ± SE.

Figure 3

Effect sizes given as mean ± SE for the spatial relations–object matching contrast within each ROI. Dark-outlined columns denote effect sizes that are consistently different from zero across conditions (p < .05).

Figure 4

fMRI results in the whole-brain analysis for the contrast of spatial relations–object matching, t = 3.5.

Figure 5

Example stimuli for the (A) categorical matching and the (B) coordinate matching tasks. Figure object being located indicated by the arrow. Original in color.

Figure 6

Behavioral performance of patient groups on the categorical and coordinate spatial tasks (mean ± SEM).

Figure 7

VLSM maps for LHD and RHD groups on the (A) categorical matching task and (B) coordinate matching task. These maps are colored depictions of t scores significant at a level of p < .05 on tests evaluating behavioral performance on a voxel-by-voxel basis. Colored areas thus represent areas where damage is predictive of the behavioral deficit observed in that group.

Figure 8

VLSM maps for LHD and RHD groups using residual analyses (A) deficits on categorical matching not accounted for by coordinate matching performance and (B) coordinate matching not accounted for by categorical matching. These maps are colored depictions of t scores significant at a level of p < .05 on tests evaluating behavioral performance on a voxel-by-voxel basis. Colored areas thus represent areas where damage is predictive of the unique behavioral deficit.