Neural Representations of Faces and Body Parts in Macaque and Human Cortex: A Comparative fMRI Study

Abstract

Single-cell studies in the macaque have reported selective neural responses evoked by visual presentations of faces and bodies. Consistent with these findings, functional magnetic resonance imaging studies in humans and monkeys indicate that regions in temporal cortex respond preferentially to faces and bodies. However, it is not clear how these areas correspond across the two species. Here, we directly compared category-selective areas in macaques and humans using virtually identical techniques. In the macaque, several face- and body part-selective areas were found located along the superior temporal sulcus (STS) and middle temporal gyrus (MTG). In the human, similar to previous studies, face-selective areas were found in ventral occipital and temporal cortex and an additional face-selective area was found in the anterior temporal cortex. Face-selective areas were also found in lateral temporal cortex, including the previously reported posterior STS area. Body part-selective areas were identified in the human fusiform gyrus and lateral occipitotemporal cortex. In a first experiment, both monkey and human subjects were presented with pictures of faces, body parts, foods, scenes, and man-made objects, to examine the response profiles of each category-selective area to the five stimulus types. In a second experiment, face processing was examined by presenting upright and inverted faces. By comparing the responses and spatial relationships of the areas, we propose potential correspondences across species. Adjacent and overlapping areas in the macaque anterior STS/MTG responded strongly to both faces and body parts, similar to areas in the human fusiform gyrus and posterior STS. Furthermore, face-selective areas on the ventral bank of the STS/MTG discriminated both upright and inverted faces from objects, similar to areas in the human ventral temporal cortex. Overall, our findings demonstrate commonalities and differences in the wide-scale brain organization between the two species and provide an initial step toward establishing functionally homologous category-selective areas.

Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

“…The mid-STS area with the connectivity profile most similar to human TPJ is close to the area whose gray matter density has previously been shown to be positively modulated by macaques' social group size (25). Macaque mid-STS is involved in the processing of social stimuli, particularly faces but also body parts (19,26). This demonstrates that one of the macaque brain areas specialized for facial and body part processing and human TPJ participate in similar distributed neural systems in both species and suggests they share a common precursor.…”

“…Although responses to faces have been demonstrated repeatedly in both species (16,19), more complicated social tasks have yet to be reported in the macaque. Moreover, there is still an ongoing debate as to whether the two species are capable of similar social tasks-the ability of macaques to engage in ToM has been questioned, as has even the possibility of resolving this debate using behavioral experiments (20).…”

Neuronal correlates of a visual “sense of number” in primate parietal and prefrontal cortices

“…However, because adaptation is not restricted to primary visual attributes, but also observed for high-level visual categories such as faces (27), the category visual numerosity may alternatively be appreciated as a special perceptual category represented spontaneously in a dedicated parietofrontal network. Other complex visual categories are also represented in the primate visual system up to the frontal lobe in a relatively specialized fashion: faces, places, and body parts appear to have dedicated neural substrates for their representation (28,29,30,31). Numerosity may thus be another visual category that is processed hierarchically, not within the ventral visual stream like faces, places, and body parts, but within the dorsal visual stream.…”

Elements for a Neural Theory of the Processing of Dynamic Faces

“…The same regions contain neurons that are selective for body shapes and movements (Barraclough, Xiao, Oram, & Perrett, 2006;Bruce, Desimone, & Gross, 1986;Oram & Perrett, 1996;Puce & Perrett, 2003;Vangeneugden, Pollick, & Vogels, 2008). Similarly, areas selective for the recognition of faces, bodies, and their movements have been localized in the STS and the temporal cortex of humans, partially in close spatial neighborhood (Grossman & Blake, 2002;Kanwisher, McDermott, & Chun, 1997;Peelen & Downing, 2007;Pinsk et al, 2009Pinsk et al, , 2005.…”

“…This idea seems consistent with the fact that face and body-selective regions are often located in close neighborhood in the visual cortex. In monkeys, neurons selective for faces have been found in the superior temporal sulcus and the temporal cortex (e.g., Desimone, Albright, Gross, & Bruce, 1984;Pinsk et al, 2009;Pinsk, DeSimone, Moore, Gross, & Kastner, 2005;Tsao, Freiwald, Knutsen, Mandeville, & Tootell, 2003). (See chapters 8, 9, and 11 for further details.)…”