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Faces and objects in macaque cerebral cortex

Abstract

How are different object categories organized by the visual system? Current evidence indicates that monkeys and humans process object categories in fundamentally different ways. Functional magnetic resonance imaging (fMRI) studies suggest that humans have a ventral temporal face area, but such evidence is lacking in macaques. Instead, face-responsive neurons in macaques seem to be scattered throughout temporal cortex, with some relative concentration in the superior temporal sulcus (STS). Here, using fMRI in alert fixating macaque monkeys and humans, we found that macaques do have discrete face-selective patches, similar in relative size and number to face patches in humans. The face patches were embedded within a large swath of object-selective cortex extending from V4 to rostral TE. This large region responded better to pictures of intact objects compared to scrambled objects, with different object categories eliciting different patterns of activity, as in the human. Overall, our results suggest that humans and macaques share a similar brain architecture for visual object processing.

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Figure 1: Object-selective areas in the macaque and human.
Figure 2: Face-selective patches in the human and macaque.
Figure 3: Regions of maximal and relative category selectivity.
Figure 4: The information content of distributed activity patterns in different brain regions.

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Acknowledgements

We wish to thank R. Desimone, N. Kanwisher, K.S. Saleem, Y. Sasaki, W. Vanduffel and D.C. Van Essen for their comments on the manuscript and valuable discussions. We are also grateful to W. Vanduffel and L. Wald for setting up the monkey fixation system, to D.C. Van Essen for help with using CARET, and to D. Greve for help with using FSFAST. This study was supported by the National Center for Research Resources (P41RR14075), the Mental Illness and Neuroscience Discovery Institute, and grants from the National Institutes of Health (R01 MH67529 A01 and R01 EB00790 A01).

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Correspondence to Doris Y Tsao.

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Supplementary information

Supplementary Fig. 1.

(a) Examples of the face and object stimuli. (b) Fourier-phase scrambled versions of images in the first row of a. (c) Grid-scrambled images. (d) Line drawings. (e) Monkey faces (used for Fig. 2e and Supplementary Fig. 4). (JPG 112 kb)

Supplementary Fig. 2.

(a,b) Areas more strongly activated by intact objects than by Fourier-scrambled objects in two monkeys ("M1" and "M2", respectively). For all slice data, the left half of each slice represents the left hemisphere. (c,d) Intact versus Fourier-scrambled object activation in monkey M2, imaged with MION contrast agent. Although MION increases signal-to-noise ratio several-fold18,20, the overall activation pattern remained the same. In (c), activation is rendered on folded and inflated views of the left hemisphere. In (d), the same functional data is overlaid on the raw functional slices (thus averting any "registration errors"). In MION images, major sulci are directly visible in the functional slices. Sulcal abbreviations: lu, lunate; ios, inferior occipital; ips, intraparietal; ots, occipito-temporal; pmt, posterior middle temporal; amt, anterior middle temporal; sts, superior temporal; lf, lateral fissure; cs, central; cgs, cingulated; arsp, arcuate spur; ias, inferior arcuate; sas, superior arcuate; ps, principal. (JPG 95 kb)

Supplementary Fig. 3.

Face-specific patches in caudal TE imaged in 10 experimental sessions spanning almost six months. In (a), (b), (d), (e), and (i), the stimulus sequence consisted of repeating cycles of {scrambled faces, faces, scrambled objects, objects}, with object epochs consisting of hands, fruits, technological objects, or bodies. In (c), (f), (g), and (h), the stimulus consisted of a fully randomized presentation sequence in which each of the five non-face stimulus categories were presented just as frequently as faces. In (f), MION contrast agent was used. In (i), the stimuli were line drawings of faces and objects. In (k), the face stimuli were pictures of macaque faces. In (j), a simple fixation task was performed instead of a foveal bar task, and only time points in which fixation was maintained within a 2° window were used. Despite these differences in experimental design, the pattern of face-selective patches remained remarkably consistent across different days. Best efforts were made to align the anterior-posterior position of the slices from different days, but since the slice separation was 1.25 mm, there may be a ±0.63 mm offset between slices in the same column. (JPG 109 kb)

Supplementary Fig. 4.

Consistency of face-selective patches across three monkeys. (a) Face patches from monkey M1 (same data as in Fig. 2b), rendered on raw functional slices. (b) Face-selective patches from monkey M2, derived using monkey faces versus objects. (c) Face patches from monkey M3 (who had never seen any of the face or object stimuli prior to scanning), derived using the exact same stimulus as in (a). (d) The same data as in (c), but without any spatial smoothing. (JPG 47 kb)

Supplementary Fig. 5.

A possible homology between the macaque face patches and the FFA. (a) Macaque face patches mapped from the individual hemisphere to the macaque atlas and displayed on the intact right hemisphere surface (left) and a flat map of the entire hemisphere (middle). The macaque atlas was registered to a human atlas using surface-based registration and landmarks based on likely functional homologies, including visual areas V1, V2, and MT27, and the deformed macaque face patches are displayed on the human right hemisphere flat map (right). (b) The location of the macaque face patches relative to reported foci of face-specific activity (green squares) and classical human visual areas. In the human map, the registered macaque face patch appears very close to the human FFA as projected to the cortical surface based on its published stereotaxic (Talairach) coordinates21. (JPG 19 kb)

Supplementary Fig. 6.

Analysis of distributed response patterns to different object categories (as in Fig. 4c), (a) without spatial smoothing, and (b) restricted to the 30 most visually-activated voxels in each region. See Results for details. (GIF 104 kb)

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Tsao, D., Freiwald, W., Knutsen, T. et al. Faces and objects in macaque cerebral cortex. Nat Neurosci 6, 989–995 (2003). https://doi.org/10.1038/nn1111

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