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Interspecies activity correlations reveal functional correspondence between monkey and human brain areas

Abstract

Evolution-driven functional changes in the primate brain are typically assessed by aligning monkey and human activation maps using cortical surface expansion models. These models use putative homologous areas as registration landmarks, assuming they are functionally correspondent. For cases in which functional changes have occurred in an area, this assumption prohibits to reveal whether other areas may have assumed lost functions. Here we describe a method to examine functional correspondences across species. Without making spatial assumptions, we assessed similarities in sensory-driven functional magnetic resonance imaging responses between monkey (Macaca mulatta) and human brain areas by temporal correlation. Using natural vision data, we revealed regions for which functional processing has shifted to topologically divergent locations during evolution. We conclude that substantial evolution-driven functional reorganizations have occurred, not always consistent with cortical expansion processes. This framework for evaluating changes in functional architecture is crucial to building more accurate evolutionary models.

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Figure 1: Detection of activity correlations between monkeys and humans.
Figure 2: Intersubject correlation of brain activity during natural vision.
Figure 3: Intra- and interspecies activity correlation from monkey areas PITd and CITd.
Figure 4: Intra- and interspecies activity correlation maps (FDR of q < 0.001) from monkey areas AIP and V3A.
Figure 5: Interspecies activity correlations between monkey and human areas.

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Acknowledgements

We thank C. Fransen, C. Van Eupen and A. Coeman for animal training and care; J.T. Arsenault, K. Nelissen, O. Joly, H. Kolster, W. Depuydt, G. Meulemans, P. Kayenbergh, M. De Paep, M. Docx and I. Puttemans for technical assistance; and S. Raiguel for his comments on the manuscript. This work received support from European Union Seventh Framework Programme FWP-200728, InterUniversity Attraction Pole 6/29, Programme Financing PFV/10/008, Geconcerteerde Onderzoeks Actie 10/19, Impulsfinanciering Zware Apparatuur and Hercules funding of the Katholieke Universiteit Leuven, Fonds Wetenschappelijk Onderzoek–Vlaanderen G062208N10, G083111N10 and G043912N, National Science Foundation BCS-0745436 and Geneeskundige Stichting Koningin Elisabeth prize “Janine en Jacques Delaruelle.” D.M. is postdoctoral fellow of the Fonds Wetenschappelijk Onderzoek–Vlaanderen. The Martinos Center for Biomedical Imaging is supported by National Center for Research Resources grant P41RR14075.

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W.V., M.C., G.L.R., D.M. and G.A.O. designed the research; D.M., V.B. and M.G.P. collected the data; D.M. analyzed the data under the supervision of U.H. and W.V.; D.M. and W.V. wrote the first draft of the manuscript, which all authors revised and approved.

Corresponding author

Correspondence to Wim Vanduffel.

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The authors declare no competing financial interests.

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Supplementary Figures 1–9, Supplementary Table 1 and Supplementary Note (PDF 4975 kb)

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Mantini, D., Hasson, U., Betti, V. et al. Interspecies activity correlations reveal functional correspondence between monkey and human brain areas. Nat Methods 9, 277–282 (2012). https://doi.org/10.1038/nmeth.1868

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