Conceptual object representations in human anterior temporal cortex

Abstract

Interaction with everyday objects requires the representation of conceptual object properties, such as where and how an object is used. What are the neural mechanisms that support this knowledge? While research on semantic dementia has provided evidence for a critical role of the anterior temporal lobes (ATLs) in object knowledge, fMRI studies using univariate analysis have primarily implicated regions outside the ATL. In the present human fMRI study we used multivoxel pattern analysis to test whether activity patterns in ATLs carry information about conceptual object properties. Participants viewed objects that differed on two dimensions: where the object is typically found (in the kitchen or the garage) and how the object is commonly used (with a rotate or a squeeze movement). Anatomical region-of-interest analyses covering the ventral visual stream revealed that information about the location and action dimensions increased from posterior to anterior ventral temporal cortex, peaking in the temporal pole. Whole-brain multivoxel searchlight analysis confirmed these results, revealing highly significant and regionally specific information about the location and action dimensions in the anterior temporal lobes bilaterally. In contrast to conceptual object properties, perceptual and low-level visual properties of the objects were reflected in activity patterns in posterior lateral occipitotemporal cortex and occipital cortex, respectively. These results provide fMRI evidence that object representations in the anterior temporal lobes are abstracted away from perceptual properties, categorizing objects in semantically meaningful groups to support conceptual object knowledge.

Figure 1.

Schematic of analysis approach. Information about conceptual object properties was assessed by cross-correlating multivoxel fMRI activity patterns evoked by the four different object groups (illustrated by the colored vectors). Information about object location was computed by subtracting the average correlation between objects that differed in location and action (red diagonal comparisons) from the average correlation between objects with the same location (green vertical comparisons). Similarly, information about object action was computed by subtracting the average correlation between objects that differed in location and action (red diagonal comparisons) from the average correlation between objects with the same action (blue horizontal comparisons).

Figure 2.

Results in ventral stream regions of interest. a, Conceptual information. Significant information about object location (light green bars) and object action (dark green bars) was found in the two most anterior ROIs of the ventral stream, BA20 and BA38. Conceptual information was computed as shown in Figure 1. b, Perceptual information. Response patterns in BA37 carried information about subjectively rated perceptual similarity of the objects. Perceptual information reflects the correlation between neural similarity and perceptual similarity. c, Pixelwise information. Response patterns in the three most posterior ROIs, BA17, BA18, and BA19, carried information about the pixelwise similarity of the objects. Pixelwise information reflects the correlation between neural similarity and pixelwise similarity. Error bars indicate SEM.

Figure 3.

Pixelwise, perceptual, and conceptual information (location, action) for each ROI, separately for both tasks, is given. There were no significant differences between the tasks for any of the information measures in any of the ROIs (t₍₂₅₎ < 1.5; p > 0.14, for all tests). Error bars indicate SEM.

Figure 4.

Results of whole-brain multivoxel searchlight analyses. a, Conceptual information. Information about conceptual object properties (location, action) was found in bilateral anterior temporal cortex. Conceptual information was computed as shown in Figure 1. b, Perceptual information. Information about perceptual object properties was found in bilateral occipitotemporal cortex. Perceptual information was computed by correlating neural similarity and perceptual similarity matrices. c, Pixelwise information. Information about pixelwise image properties was found in bilateral occipital cortex. Pixelwise information was computed by correlating neural similarity and pixelwise similarity matrices. Results were overlaid on the group-average anatomical scan and thresholded at p < 0.05 (Bonferroni corrected).