Visual processing of manipulable objects in the ventral stream is modulated by inputs from parietal action systems

Abstract

Functional object use requires the integration of visuomotor representations processed in the dorsal visual pathway with representations of surface texture and material composition of objects, processed in the ventral visual pathway. Do regions in the ventral visual pathway project outputs to dorsal visual pathway action systems, or are the outputs of the dorsal visual pathway communicated to the ventral visual pathway to modulate processing? And what are the white matter pathways that mediate structural connectivity in support of functional object use? Here we show that the left inferior parietal cortex, a region within the dorsal visual pathway, exerts a direct effect on neural responses in ventral occipital-temporal cortex during visual processing of manipulable objects. We studied a series of consecutively enrolled participants in the pre-operative phase of their neurosurgical care (N = 109) with lesions principally distributed throughout the left hemisphere. Participants completed an object processing category localizer functional MRI experiment in which they viewed images of manipulable objects, animals, faces, and places. We then used Voxel-based Lesion-Activity Mapping (VLAM), a technique in which functional responses in a region-of-interest are used to predict variance in voxel-wise lesion incidence throughout the brain. In the VLAM analyses performed here, we found that lesions to the left anterior intraparietal sulcus and left supramarginal gyrus, two inferior parietal regions known to support object-directed grasping and manipulation, respectively, cause reduced neural responses for manipulable objects (compared to faces, places and animals) in the fusiform gyrus. Parietal lesions do not affect neural responses during visual processing of places in the same region of the fusiform gyrus, even though places elicit stronger responses in the fusiform gyrus than manipulable objects. Seventy-five of 109 participants took part in a common diffusion MRI protocol, permitting a connectome-wide analyses relating white matter fiber integrity to the strength of functional responses for manipulable objects in the left fusiform gyrus. This analysis demonstrated that the descending portion of the left arcuate fasciculus mediates parietal-totemporal lobe connectivity for manipulable objects, supporting the integration of action representations with conceptual and perceptual attributes of objects. By combining voxel-based and connectome-wide lesion-symptom mapping methods with functional MRI, we have demonstrated that structural connectivity to dorsal visual pathway areas supporting skilled manual action shape category-specific neural responses for manipulable objects within the ventral visual pathway.

Keywords: Object-directed action; connectome-based lesion-activity mapping; left inferior parietal lobule; left medial fusiform gyrus; manipulable objects; voxel-based lesion-activity mapping.

Figure 1.. Preferences for manipulable objects and places in left VTC. A., C.

Spheres 3 mm in diameter represent the participant-specific manipulable object-preferring voxels localized using all runs. B., D. A leave-one-out cross-validation approach used a spherical region-of-interest (ROI) localized using N-1 runs of data to extract manipulable object preferences from the Nth run using the contrast of ‘Tools > [Animals, Faces, and Places]’ (equally weighted). This procedure was iterated N times and averaged across N data folds to derive a cross-validated t-value for manipulable objects. The same ROIs were used to obtain cross-validated t-value for place stimuli using the contrast of ‘Places > [Animals, Faces, and Tools]’ (equally weighted).

Figure 2.. VLAM analysis of manipulable objects and places in left VTC.

A. Reduced preferences for manipulable objects in left VTC were associated with lesion presence in the left SMG, aIPS, parietal operculum, angular gyrus, and the posterior middle temporal gyrus (red-to-yellow). An overlapping lesion site in the posterior temporal lobe was also associated with reduced place preferences (magenta), whereas lesions to anterior portions of the temporal lobe, thalamus, insula, hippocampus, and posterior fusiform gyrus were uniquely associated with place preferences in left VTC (blue-to-green).

Figure 3.. Voxelwise comparison between VLAM analyses of manipulable objects and places in the left VTC.

Values in each VLAM map in Figure 2 are z-scores; thus, we performed a subtraction analysis in each voxel to quantify the difference between the result for manipulable objects subtracting out the result for places. A 1,000 iteration permutation analysis followed, in which the VLAM maps were scrambled prior to subtracting the place VLAM map from the manipulable object VLAM map. The voxelwise difference scores of the true data were then z-scored against the mean permutation-derived voxelwise difference scores. The voxelwise comparison analysis identifies the left SMG, aIPS, posterior middle temporal gyrus and underlying white matter as a VLAM-identified lesion site that was significantly greater for manipulable objects. By contrast, lesions to the anterior inferior, middle, and superior temporal gyri, as well as the thalamus, insula, hippocampus, and posterior fusiform gyrus, were associated with a stronger VLAM result for places.

Figure 4.. Connectome-based lesion-activity mapping in the left VTC.

(A) The connectometry analysis of manipulable objects (red, yellow) and places (blue) identified overlapping fibers in the left inferior fronto-occipital fasciculus, the left inferior longitudinal fasciculus, and the left middle longitudinal fasciculus. By contrast, the arcuate fasciculus (yellow) was identified as a white matter pathway in which reduced FA was associated with reduced responses for manipulable objects in left VTC. (B) There is convergence between the VLAM-identified aIPS and SMG lesion site (red) and the connectometry-identified left arcuate fasciculus (yellow; axial slice Z = 30). Inferior to that is a lesion site in the posterior middle temporal gyrus that overlaps with the inferior fronto-occipital fasciculus (green), inferior longitudinal fasciculus (blue), and middle longitudinal fasciculus (purple).