Gaze following in Archosauria—Alligators and palaeognath birds suggest dinosaur origin of visual perspective taking

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Abstract

Taking someone else’s visual perspective marks an evolutionary shift in the formation of advanced social cognition. It enables using others’ attention to discover otherwise hidden aspects of the surroundings and is foundational for human communication and understanding of others. Visual perspective taking has also been found in some other primates, a few songbirds, and some canids. However, despite its essential role for social cognition, visual perspective taking has only been fragmentedly studied in animals, leaving its evolution and origins uncharted. To begin to narrow this knowledge gap, we investigated extant archosaurs by comparing the neurocognitively least derived extant birds—palaeognaths—with the closest living relatives of birds, the crocodylians. In a gaze following paradigm, we showed that palaeognaths engage in visual perspective taking and grasp the referentiality of gazes, while crocodylians do not. This suggests that visual perspective taking originated in early birds or nonavian dinosaurs—likely earlier than in mammals.

Abstract

Visual perspective taking evolved earlier in dinosaurs than mammals.

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Cerebellum and nonmotor function.

Julie A. Fiez, P L Strick, R Dum (2008)

Does the cerebellum influence nonmotor behavior? Recent anatomical studies demonstrate that the output of the cerebellum targets multiple nonmotor areas in the prefrontal and posterior parietal cortex, as well as the cortical motor areas. The projections to different cortical areas originate from distinct output channels within the cerebellar nuclei. The cerebral cortical area that is the main target of each output channel is a major source of input to the channel. Thus, a closed-loop circuit represents the major architectural unit of cerebro-cerebellar interactions. The outputs of these loops provide the cerebellum with the anatomical substrate to influence the control of movement and cognition. Neuroimaging and neuropsychological data supply compelling support for this view. The range of tasks associated with cerebellar activation is remarkable and includes tasks designed to assess attention, executive control, language, working memory, learning, pain, emotion, and addiction. These data, along with the revelations about cerebro-cerebellar circuitry, provide a new framework for exploring the contribution of the cerebellum to diverse aspects of behavior.

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Internal models in the cerebellum.

D. M. Wolpert, R Miall, M. Kawato (1998)

This review will focus on the possibility that the cerebellum contains an internal model or models of the motor apparatus. Inverse internal models can provide the neural command necessary to achieve some desired trajectory. First, we review the necessity of such a model and the evidence, based on the ocular following response, that inverse models are found within the cerebellar circuitry. Forward internal models predict the consequences of actions and can be used to overcome time delays associated with feedback control. Secondly, we review the evidence that the cerebellum generates predictions using such a forward model. Finally, we review a computational model that includes multiple paired forward and inverse models and show how such an arrangement can be advantageous for motor learning and control.

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Birds have primate-like numbers of neurons in the forebrain.

Seweryn Olkowicz, Martin Kocourek, Radek K Lucan … (2016)

Some birds achieve primate-like levels of cognition, even though their brains tend to be much smaller in absolute size. This poses a fundamental problem in comparative and computational neuroscience, because small brains are expected to have a lower information-processing capacity. Using the isotropic fractionator to determine numbers of neurons in specific brain regions, here we show that the brains of parrots and songbirds contain on average twice as many neurons as primate brains of the same mass, indicating that avian brains have higher neuron packing densities than mammalian brains. Additionally, corvids and parrots have much higher proportions of brain neurons located in the pallial telencephalon compared with primates or other mammals and birds. Thus, large-brained parrots and corvids have forebrain neuron counts equal to or greater than primates with much larger brains. We suggest that the large numbers of neurons concentrated in high densities in the telencephalon substantially contribute to the neural basis of avian intelligence.

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Author and article information

Contributors

Claudia Zeiträg:

ORCID: https://orcid.org/0000-0001-6056-7437

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Stephan A. Reber:

ORCID: https://orcid.org/0000-0001-8015-2538

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: Writing - original draftRole: Writing - review & editing

Mathias Osvath:

ORCID: https://orcid.org/0000-0002-7873-0930

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: May 2023

Publication date (Electronic, pub): 19 May 2023

Volume: 9

Issue: 20

Electronic Location Identifier: eadf0405

Affiliations

[1]Department of Philosophy and Cognitive Science, Lund University, Lund, Sweden.

Author notes

[* ]Corresponding author. Email: claudia.zeitrag@ 123456lucs.lu.se

Author information

Claudia Zeiträg https://orcid.org/0000-0001-6056-7437

Stephan A. Reber https://orcid.org/0000-0001-8015-2538

Mathias Osvath https://orcid.org/0000-0002-7873-0930

Article

Publisher ID: adf0405

DOI: 10.1126/sciadv.adf0405

PMC ID: 10198628

PubMed ID: 37205749

SO-VID: 9b66221b-35fd-451a-b389-ff204a573805

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

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This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 05 October 2022

Date accepted : 17 April 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Award ID: 2019-03265

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Award ID: 2021-02973

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Award ID: 2021-01650

Funded by: LMK;

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Copyeditor Penchie Limbo

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Gaze following in Archosauria—Alligators and palaeognath birds suggest dinosaur origin of visual perspective taking

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Most cited references 65

Cerebellum and nonmotor function.

Internal models in the cerebellum.

Birds have primate-like numbers of neurons in the forebrain.

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