Proceedings of the Royal Society B: Biological Sciences
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Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight

Amy Balanoff

Amy Balanoff

Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

abalano2@jhmi.edu

Contribution: Conceptualization, Formal analysis, Funding acquisition, Investigation, Writing – original draft, Writing – review & editing

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Elizabeth Ferrer

Elizabeth Ferrer

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

Samuel Merritt University, Oakland, CA 94609, USA

Contribution: Conceptualization, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing

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Lemise Saleh

Lemise Saleh

Department of Biomedical Engineering and Radiology, Stony Brook University, Stony Brook, NY 11794, USA

Contribution: Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing

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Paul M. Gignac

Paul M. Gignac

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

Department of Cellular and Molecular Medicine, University of Arizona College of Medicine, Tucson, AZ 85724, USA

Contribution: Conceptualization, Funding acquisition, Writing – original draft, Writing – review & editing

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M. Eugenia L. Gold

M. Eugenia L. Gold

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

Department of Biology, Suffolk University, Boston, MA 02108, USA

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Jesús Marugán-Lobón

Jesús Marugán-Lobón

Unidad de Paleontología, Departamento Biología, Universidad Autónoma de Madrid, 28049 Cantoblanco (Madrid), Spain

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Mark Norell

Mark Norell

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

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David Ouellette

David Ouellette

Weill Cornell Medical College, New York, NY 10065, USA

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Michael Salerno

Michael Salerno

Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA

Contribution: Conceptualization, Formal analysis, Investigation, Methodology, Writing – review & editing

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Akinobu Watanabe

Akinobu Watanabe

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, NY 11568, USA

Life Sciences Department, Vertebrates Division, Natural History Museum, London SW7 5BD, UK

Contribution: Formal analysis, Funding acquisition, Writing – original draft, Writing – review & editing

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Shouyi Wei

Shouyi Wei

Department of Physics, New York Proton Center, New York, NY 10035, USA

Contribution: Formal analysis, Investigation, Writing – review & editing

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Gabriel Bever

Gabriel Bever

Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

gbever1@jhmi.edu

Contribution: Conceptualization, Formal analysis, Funding acquisition, Investigation, Writing – original draft, Writing – review & editing

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Paul Vaska

Paul Vaska

Department of Biomedical Engineering and Radiology, Stony Brook University, Stony Brook, NY 11794, USA

paul.vaska@stonybrookmedicine.edu

Contribution: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

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    The evolution of flight is a rare event in vertebrate history, and one that demands functional integration across multiple anatomical/physiological systems. The neuroanatomical basis for such integration and the role that brain evolution assumes in behavioural transformations remain poorly understood. We make progress by (i) generating a positron emission tomography (PET)-based map of brain activity for pigeons during rest and flight, (ii) using these maps in a functional analysis of the brain during flight, and (iii) interpreting these data within a macroevolutionary context shaped by non-avian dinosaurs. Although neural activity is generally conserved from rest to flight, we found significant increases in the cerebellum as a whole and optic flow pathways. Conserved activity suggests processing of self-movement and image stabilization are critical when a bird takes to the air, while increased visual and cerebellar activity reflects the importance of integrating multimodal sensory information for flight-related movements. A derived cerebellar capability likely arose at the base of maniraptoran dinosaurs, where volumetric expansion and possible folding directly preceded paravian flight. These data represent an important step toward establishing how the brain of modern birds supports their unique behavioural repertoire and provide novel insights into the neurobiology of the bird-like dinosaurs that first achieved powered flight.

    Footnotes

    These authors contributed equally to this study.

    Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.7021311.

    References