Domain-Specific Diaschisis: Lesions to Parietal Action Areas Modulate Neural Responses to Tools in the Ventral Stream

Abstract

Neural responses to small manipulable objects ("tools") in high-level visual areas in ventral temporal cortex (VTC) provide an opportunity to test how anatomically remote regions modulate ventral stream processing in a domain-specific manner. Prior patient studies indicate that grasp-relevant information can be computed about objects by dorsal stream structures independently of processing in VTC. Prior functional neuroimaging studies indicate privileged functional connectivity between regions of VTC exhibiting tool preferences and regions of parietal cortex supporting object-directed action. Here we test whether lesions to parietal cortex modulate tool preferences within ventral and lateral temporal cortex. We found that lesions to the left anterior intraparietal sulcus, a region that supports hand-shaping during object grasping and manipulation, modulate tool preferences in left VTC and in the left posterior middle temporal gyrus. Control analyses demonstrated that neural responses to "place" stimuli in left VTC were unaffected by lesions to parietal cortex, indicating domain-specific consequences for ventral stream neural responses in the setting of parietal lesions. These findings provide causal evidence that neural specificity for "tools" in ventral and lateral temporal lobe areas may arise, in part, from online inputs to VTC from parietal areas that receive inputs via the dorsal visual pathway.

Keywords: anterior intraparietal sulcus; dorsal stream; fMRI; manipulable objects; neurosurgery; supramarginal gyrus; tools; ventral stream; voxel-based lesion-activity mapping; voxel-based lesion-symptom mapping.

Figure 1.

ROI analysis of ventral temporal tool-preferring voxels. (A) Subject-specific left ventral temporal tool-preferring ROIs are represented as spheres (6 mm diameter). Subject-specific tool-preferring ROIs were defined using half of the data (e.g., even runs) from each participant, and the remaining half the data (i.e., odd runs) from that participant were used to calculate category-preferences at the single-subject level (with averaging across the data folds). The average location for the neurosurgery participant group (mean Talairach X, Y, Z: –27, –55, –17) was in close proximity (Euclidean distance, 3 mm) to the average location in the healthy adult group (mean Talairach X, Y, Z: –27, –58, –17). Plotted in the bar graphs are contrast-weighted t-values for each category versus the fixation baseline. (B) The amplitude of category preferences in single-subject tool-preferring ventral temporal cortex ROIs were obtained in the neurosurgery group (using half of the data to define, the other half to measure). Plotted in the bar graphs are contrast-weighted t-values for each category versus the fixation baseline. Dots in all bar graphs represent individual participants.

Figure 2.

Voxel-based Lesion Activity Mapping (VLAM) showing that lesions to aIPS modulate neural responses to tools in left ventral temporal cortex. (A) Lesions to the left supramarginal gyrus and left anterior intraparietal sulcus, and adjacent white matter areas, are inversely related to tool preferences in left ventral temporal cortex (red-to-yellow color-scale). All partial correlation coefficient values plotted in the map (regressing lesion volume) survive cluster correction (cluster correction using AlphaSim, minimum cluster size of 66 voxels, with an initial alpha level of P < 0.01, uncorrected). To test for the specificity of parietal lesions modulating tool responses in left ventral temporal cortex, we repeated the analysis using place preferences as measured from the same tool-preferring ventral temporal ROIs (again, regressing lesion volume). The results, plotted on the blue-to-green color-scale, identify temporal lobe regions but importantly do not identify parietal areas (all values survive cluster correction, with a minimum cluster size of 68 voxels, initial alpha of P < 0.01, uncorrected). The same results were obtained when not regressing lesion volume, and when measuring tool- and place-preferences using alternative baselines (see Supplementary Fig. 2). (B) A direct comparison of VLAM results for tools and those for places identifies the left aIPS and supramarginal gyrus. Plotted in Figure 2B are negative z-values (greater VLAM effect for tools than places; minimum z value = –1.96, P < 0.05, two-tailed). We note that there were no sites associated with VLAM effects for places that were significantly greater than VLAM effects for tools.

Figure 3.

Confirmation that the VLAM analysis identifies the tool-preferring aIPS in the healthy adult group. (A) The overlap between the Voxel-based Lesion Activity Mapping (VLAM) analysis (red-to-yellow color-scale) and tool preferences (Tools > [Animals, Faces, & Places]) (weighted equally) in the healthy adult group (blue-to-white color-scale) was computed. Overlap was maximal at the left aIPS. (B) We independently defined the left aIPS using NeuroSynth and created an aIPS sphere centered on the peak Talairach coordinate (XYZ = −47 −30 38, 6 mm in diameter). Category-preferences for that ROI were extracted for the healthy adult group, and are plotted in the bar graph. The results indicate robust tool responses (one-sample t-test versus fixation baseline, t(37) = 2.75, P < 0.01) and tool-preferences (“Tools > [Animals, Faces, Places]” (“T > AFP”), t(37) = 6.14, P < 0.001). (C) In a final test, we extracted category-preferences from the healthy participants for the ROI defined as overlapping the VLAM analysis and tool-preferences in the healthy participants, using a split-half analysis to maintain independence of voxel definition and test. Specifically, using the healthy adult dataset we computed the whole-brain contrast of “Tools > [Animals, Faces, & Places]” using half the data (e.g., even runs) and determined overlap between that map (FDR corrected, q < 0.05) and the VLAM results; category-preferences were extracted for voxels identified as overlapping, using the left-out half of data (i.e., odd runs) from the healthy participants (to estimate category-preferences). This procedure was repeated using the other half of the healthy data to define a whole-brain map of tool preferences (e.g., odd runs) and extracting data for the left-out half (i.e., even runs). The results are plotted in the bar graph and demonstrate nearly the exact pattern obtained using the Neurosynth coordinates for aIPS. There were robust tool responses (one-sample t-test versus fixation baseline, t(37) = 3.34, P < 0.01) and tool-preferences (“Tools > [Animals, Faces, Places]” (“T > AFP”), t(37) = 7.78, P < 0.001). Note that the aIPS region identified by the overlap analysis was anatomically proximal (odd runs, 7 mm Euclidean distant; even runs, 7.3 mm Euclidean distant) to the Neurosynth-defined left aIPS peak, indicating that a common set of anatomical voxels are identified by independent methods for identifying the left aIPS. Dots in the bar graphs represent individual participants. ** = P < 0.01; *** = P < 0.001.

Figure 4.

Reverse Voxel-based Lesion Activity Mapping (VLAM) demonstrates tool preferences in left ventral temporal cortex and the left posterior middle temporal gyrus are modulated by left aIPS lesions. (A) A reverse VLAM analysis was carried out in which a vector of aIPS lesion presence/absence was correlated with voxelwise tool preferences (“Tools > [Animals, Faces, & Places]” (weighted equally)) to identify regions (whole-brain) in which aIPS lesions modulate tool preferences. These analyses identify voxels in the left medial fusiform gyrus (collateral sulcus), replicating prior findings (Fig. 2), and also the left posterior middle temporal gyrus. In addition, we found that tool preferences in the right posterior middle/inferior temporal gyrus were modulated in the presence of left aIPS lesions (all correlation values are significant at an alpha level of P < 0.01, uncorrected). Note the reverse VLAM maps are plotted in radiological convention.