Animacy and real-world size shape object representations in the human medial temporal lobes

Abstract

Identifying what an object is, and whether an object has been encountered before, is a crucial aspect of human behavior. Despite this importance, we do not yet have a complete understanding of the neural basis of these abilities. Investigations into the neural organization of human object representations have revealed category specific organization in the ventral visual stream in perceptual tasks. Interestingly, these categories fall within broader domains of organization, with reported distinctions between animate, inanimate large, and inanimate small objects. While there is some evidence for category specific effects in the medial temporal lobe (MTL), in particular in perirhinal and parahippocampal cortex, it is currently unclear whether domain level organization is also present across these structures. To this end, we used fMRI with a continuous recognition memory task. Stimuli were images of objects from several different categories, which were either animate or inanimate, or large or small within the inanimate domain. We employed representational similarity analysis (RSA) to test the hypothesis that object-evoked responses in MTL structures during recognition-memory judgments also show evidence for domain-level organization along both dimensions. Our data support this hypothesis. Specifically, object representations were shaped by either animacy, real-world size, or both, in perirhinal and parahippocampal cortex, and the hippocampus. While sensitivity to these dimensions differed across structures when probed individually, hinting at interesting links to functional differentiation, similarities in organization across MTL structures were more prominent overall. These results argue for continuity in the organization of object representations in the ventral visual stream and the MTL.

Keywords: animacy; category specificity; hippocampus; parahippocampal cortex; perirhinal cortex; real-world size; recognition memory.

Figure 1

Stimuli. Example objects from the 12 object categories employed. Categories were grouped into animate: faces, bodies, monkeys, insects; inanimate small: flowers, fruits, tools, musical instruments; and inanimate large: buildings, trees, vehicles, and furniture [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Task: Continuous recognition memory. An image depicting an object from 1 of the 12 categories was presented on screen for 1,200 ms. After 600 ms, a red border popped up around the image, and participants were required to respond “novel” indicating it was the first time they had seen that image, or “old” indicating that it was the second time they had seen that image [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Left: tripartite preference zones in posterior occipito‐temporal cortex (courtesy of Konkle & Carmazza 2013). Right: anatomical regions of interest examined in the medial temporal lobe, for one example participant [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Recognition memory performance for domains of interest, as measured with d′. There were no significant differences on performance between animate or inanimate objects (p = .2), or between large and small inanimate objects (p = .7)

Figure 5

Representational geometry for object‐evoked responses in the medial temporal lobe. Representational similarity matrices for the three MTL structures. Matrices show Pearson's correlations between patterns of activity evoked by each object category compared to each other object category. Note that the diagonal shows within‐category correlations across runs (each run had different exemplars from the given category). The top row shows each RSM without scaling across structures and the bottom row shows each RSM on the same scale for all structures. Note that RSM's are not symmetrical in the visualization, this is because the upper triangle shows the mean from a subset of across run correlations (i.e., cell 1,2 is condition 1 in the even runs correlated with condition 2 in the odd runs, whereas cell 2,1 is condition 1 in the odd runs correlated with condition 2 in the even runs) [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 6

Organization of object representations in the MTL. All bar plots show beta fits between model of organization tested and RSM for each MTL structure: (a) model of category representation; (b) model of animacy organization; (c) model of real‐world size for the inanimate domain.* indicates the model fit was significant with correction for multiple comparisons [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 7

Visualization of representational space. Hierarchical clustering for all object categories in each MTL structure [Color figure can be viewed at http://wileyonlinelibrary.com]