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.

Disentangling five dimensions of animacy in human brain and behaviour

“…Animate-looking (e.g., cow mug) and animate objects (e.g., cow) are dissociated in behaviour but not in the ventral visual stream measured by fMRI (Bracci et al, 2019). Chosen animacy dimensions explain variance in the ventral visual stream fMRI measurements: agency (Thorat et al, 2019), animacy (Blumenthal et al, 2018), humanlikeness (Rosenthal-von der Pütten et al, 2019), and capacity for self-movement and thought rather than face presence (Proklova & Goodale, 2020). The time course with which animacy representations emerge has been investigated with magnetoencephalography (MEG), revealing the time course of agency (Contini et al, 2019).…”

“…Recognizing animate things is essential for choosing appropriate actions as we engage the physical and social world, and can be a matter of life and death (e.g., quick recognition of a tiger in the wild). Animacy is an important representational division in nonhuman and human higher ventral visual cortical areas in the inferior temporal cortex (Kriegeskorte et al, 2008) and the medial temporal lobe (Blumenthal et al, 2018) as measured by functional magnetic resonance imaging (fMRI). Consistent with the importance of animacy perception in the classical neuropsychological literature, lesion studies established that living things are represented in dedicated regions of the cortex (Funnell & Sheridan, 1992; Ralph et al, 1998; Silveri et al, 1996).…”

Real-world size of objects serves as an axis of object space

“…𝐿𝑜𝑔𝑎𝑟𝑖𝑡ℎ𝑚𝑖𝑐: 𝑦 = ln 𝑥 (11) where x is the value of the real-world size PC, and y is the measured real-world size of objects. The scale with the best fit was taken as the relationship that best describes the data.…”

“…Third, fMRI studies on humans have revealed that the real-world size of objects is encoded in human's ventral temporal cortex, where the medial part of the occipitotemporal cortex is preferable to object with a larger size and the lateral to a smaller size (9). Finally, size information is apparently encoded independently from animacy, and they together form a tripartite organizational schema (i.e., big objects, all animals and small objects) in the ventral occipitotemporal cortex (10) and medial temporal lobe (11).…”

Real-world size of objects serves as an axis of object space

“…Third, fMRI studies on humans have revealed that the real-world size of objects is encoded in human's ventral temporal cortex, where the medial part of the occipitotemporal cortex is preferable to object with a larger size and the lateral to a smaller size 6 . Finally, size information is apparently encoded independently from animacy, and they together form a tripartite organizational schema (i.e., big objects, all animals and small objects) in the ventral occipitotemporal cortex 7 and medial temporal lobe 8 . However, the neuronal sensitivity (sensitivity criterion) to a feature is requisite, but not sufficient, for examining whether the feature serves as an axis of object space.…”