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Cited by 210Primate Behavior and EcologyEmbodied and Extended CognitionMotor Control and Adaptation

Embodied cognitive evolution and the cerebellum

Open access
Barton, Robert A.·2012·Philosophical Transactions of the Royal Society B: Biological Sciences
DOI 10.1098/rstb.2012.0112PMC PMC3385677
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Abstract

Much attention has focused on the dramatic expansion of the forebrain, particularly the neocortex, as the neural substrate of cognitive evolution. However, though relatively small, the cerebellum contains about four times more neurons than the neocortex. I show that commonly used comparative measures such as neocortex ratio underestimate the contribution of the cerebellum to brain evolution. Once differences in the scaling of connectivity in neocortex and cerebellum are accounted for, a marked and general pattern of correlated evolution of the two structures is apparent. One deviation from this general pattern is a relative expansion of the cerebellum in apes and other extractive foragers. The confluence of these comparative patterns, studies of ape foraging skills and social learning, and recent evidence on the cognitive neuroscience of the cerebellum, suggest an important role for the cerebellum in the evolution of the capacity for planning, execution and understanding of complex behavioural sequences—including tool use and language. There is no clear separation between sensory–motor and cognitive specializations underpinning such skills, undermining the notion of executive control as a distinct process. Instead, I argue that cognitive evolution is most effectively understood as the elaboration of specialized systems for embodied adaptive control.

AI snapshot

Written from the paper’s full text.

TL;DR

Barton argues that comparative brain evolution has overemphasized the neocortex and neglected the cerebellum, which contains about four times more neurons than the neocortex. Using phylogenetic comparative analyses, the paper finds correlated neocortex–cerebellum evolution plus a dissociation in which cerebellum size is more associated with extractive foraging/tool use and neocortex size with social group size, supporting an embodied, sensory–motor account of cognitive evolution.

Key findings

  • The cerebellum contains about four times more neurons than the neocortex, and volumetric ratios can mislead: the ratio of cortical to cerebellar volumes is uncorrelated with the ratio of cortical to cerebellar neurons (PGLS; λ = 0.63, t2,23 = 1.13, p = 0.27).
  • Neocortex and cerebellum show correlated evolution, but with independent contributions to brain size: regressing brain mass on body mass, neocortex, cerebellum, and their interaction gave body mass t = 8.47, p < 0.0001; neocortex t = 19.73, p < 0.0001; cerebellum t = 12.35, p < 0.0001; interaction t = 4.04, p < 0.0001; λ = 0.92, n = 298 mammal species.
  • A behavioural double dissociation was found: with the other structure controlled, neocortex size correlated with social group size (t6,36 = 3.92, p = 0.0005) but not extractive foraging (t6,36 = 1.01, p = 0.32), whereas cerebellum size correlated with extractive foraging (t6,36 = 3.59, p = 0.001) but not social group size (t6,36 = 1.33, p = 0.19).
  • For tool use, cerebellum size correlated with tool use (t5,36 = 2.04, p = 0.050) but not social group size (t6,36 = 1.47, p = 0.15), while neocortex size correlated with social group size (t6,36 = 3.98, p = 0.0003) but not tool use (t6,36 = 0.71, p = 0.48).

Methods

  • Phylogenetic comparative analyses of brain component volumes and neuron numbers, including broad patterns across mammalian orders and focused analyses within primates.
  • Main analysis used phylogenetic generalized least squares (PGLS) to incorporate phylogeny into statistical models of correlated trait evolution; further details and data are said to be in the electronic supplementary material.
  • Results are presented within discussion of key questions rather than consolidated in a single results section; key analyses include n = 298 mammal species for brain mass and primate analyses with t4,42 or t6,36 degrees of freedom.

Limitations

  • Stated: the paper says the details of the debate over whether cerebellar cognitive functions are proven are beyond its scope; comparative data on frontal lobes are relatively sparse; and direct observation of evolutionary processes is absent, so phylogenetic comparative analysis is used to investigate patterns and processes.
  • Evident from the text: the analyses are correlational/phylogenetic comparative and cannot by themselves establish causal selection pressures; several conclusions synthesize evidence from other studies, including functional imaging, clinical, and behavioural work.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1098/rstb.2012.0112

Cites

133 of 133 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

0 of 73 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § 2. Methods

    There is no correlation between body size and proportion of the brain that is cerebellum (λ = 0.93, t = 1.25, p = 0.21).

    “There is no such correlation for the cerebellum (λ = 0.93, t = 1.25, p = 0.21).”
    Quote in the paperSubstantial claim
  • Findingnone given
    § Abstract

    One deviation from the general pattern of correlated evolution is a relative expansion of the cerebellum in apes and other extractive foragers.

    “One deviation from this general pattern is a relative expansion of the cerebellum in apes and other extractive foragers.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    Once differences in the scaling of connectivity in neocortex and cerebellum are accounted for, a marked and general pattern of correlated evolution of the two structures is apparent.

    “Once differences in the scaling of connectivity in neocortex and cerebellum are accounted for, a marked and general pattern of correlated evolution of the two structures is apparent.”
    Quote in the paperSubstantial claim
  • Findingown data
    § 2. Methods

    The correlated evolution of neocortex and cerebellum is evident not just in volumes, but also in two independent data sets on numbers and densities of neurons.

    “Third, it is evident not just in terms of volumes, but also in two independent data sets on numbers and densities of neurons (figure S1 in the electronic supplementary material).”
    Quote in the paperSubstantial claim
  • Findingcitation
    § 2. Methods

    Larger cortices are increasingly made up of white rather than grey matter.

    “larger cortices are increasingly made up of white rather than grey matter (figure 1a, see also [46,47]).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [46] Zhang K., Sejnowski T. J. 2000. A universal scaling law between gray matter and white matter of cerebral cortex. Proc. Natl Acad. Sci. USA 97, 5621–5626 10.1073/pnas.090504197 (doi:10.1073/pnas.090504197) [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [47] Bush E. C., Allman J. M. 2003. The scaling of white matter to grey matter in cerebellum and neocortex. Brain Behav. Evol. 61, 1–5 10.1159/000068880 (doi:10.1159/000068880) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims. 15
  • Classified as probably not a substantial claim. 7

  • May combine two claims.

    Findingown data
    § 2. Methods

    Controlling for body mass, mammalian brain size is positively and independently correlated with both neocortex and cerebellum, and there is a significant interaction between the effects of the two structures on brain size.

    “Indeed, a phylogenetic analysis reveals that, controlling for body mass, mammalian brain size is positively and independently correlated with both neocortex and cerebellum, and also that there is a significant interaction between the effects of the two structures on brain size (PGLS, brain mass regressed on: body mass, t = 8.47, p < 0.0001; neocortex, t = 19.73, p < 0.0001; cerebellum, t = 12.35,”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation
    § 2. Methods

    The conjoint expansion of neocortex and cerebellum early in primate evolution reflects a general evolutionary trend for the two structures to evolve together, in primates and more generally during mammalian evolution.

    “This conjoint expansion of the two structures early in primate evolution reflects a general evolutionary trend for the two structures to evolve together, in primates in particular [23,26,62,67], and more generally during mammalian evolution (figure 4).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [23] Barton R. A., Harvey P. H. 2000. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058 10.1038/35016580 (doi:10.1038/35016580) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [26] Herculano-Houzel S. 2010. Coordinated scaling of cortical and cerebellar numbers of neurons. Front. Neuroanat. 4, 12 10.3389/fnana.2010.00012 (doi:10.3389/fnana.2010.00012) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [62] Smaers J. B., Steele J., Zilles K. 2011. Modeling the evolution of cortico-cerebellar systems in primates. Ann. NY Acad. Sci. 1225, 176–190 10.1111/j.1749-6632.2011.06003.x (doi:10.1111/j.1749-6632.2011.06003.x) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [67] Whiting B., Barton R. A. 2003. The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10 10.1016/S0047-2484(02)00162-8 (doi:10.1016/S0047-2484(02)00162-8) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Findingcitation
    § 2. Methods

    Cortical neuron number proportion is unrelated to brain size and unrelated to cortical volume proportion.

    “In stark contrast to the way that cortical volume proportion scales up with brain size, cortical neuron number proportion is unrelated to brain size [26] and unrelated to cortical volume proportion [25].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [26] Herculano-Houzel S. 2010. Coordinated scaling of cortical and cerebellar numbers of neurons. Front. Neuroanat. 4, 12 10.3389/fnana.2010.00012 (doi:10.3389/fnana.2010.00012) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

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      Not checked in the free run.

  • May combine two claims.

    Findingcitation
    § 2. Methods

    The same pattern is found after subtracting primary visual area V1 from total neocortex volume, emphasizing that extra-striate cortex is not 'non-visual'.

    “The same pattern is found after subtracting primary visual area V1 from total neocortex volume (λ = 0.89, r2 = 0.98, n = 42; LGN, t4,42 = 2.82, p = 0.008; cerebellum, t4,42 = 4.26, p = 0.0001), emphasizing that extra-striate cortex is not ‘non-visual’ [68].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [68] van Essen D. C., Anderson C. H., Felleman D. J. 1992. Information processing in the primate visual system: an integrated systems perspective. Science 255, 419–423 10.1126/science.1734518 (doi:10.1126/science.1734518) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Findingown data
    § 2. Methods

    Neuron density decreases as brain size increases in both neocortex and cerebellum, but the decline is significantly steeper in the neocortex.

    “Neuron density decreases as brain size increases in both neocortex (PGLS: λ = 0.83, slope = −0.23, t2,23 = 4.55, p < 0.0002) and cerebellum (PGLS: λ = 0.76, slope = −0.04, t = 2.43, p = 0.02), but the decline is significantly steeper in the neocortex (difference in PGLS coefficients: t = 3.92, p = 0.0008).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning
    § Abstract

    There is no clear separation between sensory-motor and cognitive specializations underpinning complex behavioural sequences, undermining the notion of executive control as a distinct process.

    “There is no clear separation between sensory–motor and cognitive specializations underpinning such skills, undermining the notion of executive control as a distinct process.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisereasoning
    § 1. Introduction

    There are theoretical reasons to question the assumption that intelligence evolved in a unitary way and can in principle be measured by a single, ideal comparative brain measure.

    “There are also theoretical reasons to question the underlying assumption that intelligence evolved in a unitary way and can in principle be measured by a single, ideal comparative brain measure.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § 1. Introduction

    Understanding brain evolution both contributes to and is benefited by the embodied cognition perspective.

    “Here I argue that understanding brain evolution both contributes to and is benefited by this perspective.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisecitation
    § 1. Introduction

    Cognition is best conceived as a set of processes mediating the adaptive control of bodies in environments (embodied cognition).

    “More recently, these distinctions have been broken down by the recognition that cognition is best conceived as a set of processes mediating the adaptive control of bodies in environments: the concept of embodied cognition [28–33].”
    Quote in the paperNot a substantial claim0 of 6 sources checked
    • cites [28] Damasio A. 1994. Descartes’ error: emotion, reason, and the human brain. New York, NY: Putnam [Google Scholar]

      Not checked in the free run.

    • cites [29] Chiel H. J., Beer R. D. 1997. The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci. 20, 553–557 10.1016/S0166-2236(97)01149-1 (doi:10.1016/S0166-2236(97)01149-1) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [30] Clark A. 1997. Being there: putting brain, body, and world together again. Cambridge, MA: MIT Press [Google Scholar]

      Not checked in the free run.

    • cites [31] Wilson M. 2002. Six views of embodied cognition. Psychol. Bull. Rev. 9, 625–636 10.3758/BF03196322 (doi:10.3758/BF03196322) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

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      Not checked in the free run.

    • cites [33] Barrett L., Henzi S. P., Lusseau D. 2012. Taking sociality seriously: the structure of multi-dimensional social networks as a source of information for individuals. Phil. Trans. R. Soc. B 367, 2108–2118 10.1098/rstb.2012.0113 (doi:10.1098/rstb.2012.0113) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 1. Introduction

    An excessive emphasis on the neocortex has obscured important patterns in brain evolution and led to an unwarranted neglect of the cerebellum.

    “I argue that an excessive emphasis on the neocortex has obscured important patterns in brain evolution and led to an unwarranted neglect of the cerebellum.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisenone given
    § 1. Introduction

    It is circular to argue that a particular comparative brain measure is ideal because it most strongly supports a hypothesis.

    “Indeed, it is circular to argue that a particular measure is ideal because it most strongly supports a hypothesis.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § 11. Conclusions

    There is a general tendency of neocortex and cerebellum to evolve together.

    “Whilst there are general patterns, such as the tendency of neocortex and cerebellum to evolve together, there are also significant deviations from such trends, such as visual pathway expansion in primates, and cerebellar expansion in apes.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 2. Methods

    The cerebellum is also larger and contains more neurons in primates compared to other mammals.

    “However, the cerebellum is also larger [66] and contains more neurons in primates compared to other mammals (figure 3).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [66] Barton R. A. 2000. Ecological and social factors in primate brain evolution. In On the move: how and why animals travel in groups (eds Boinski S., Garber P.), pp. 204–237 Chicago, IL: Chicago University Press [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 5. Cognitive implications

    The cerebellum is involved in sensory-motor control and learning of motor skills.

    “It has long been known that the cerebellum is involved in sensory–motor control and learning of motor skills [72,73].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [72] Glickstein M., Doron K. 2008. Cerebellum: connections and functions. Cerebellum 7, 589–594 10.1007/s12311-008-0074-4 (doi:10.1007/s12311-008-0074-4) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § 2. Methods

    These results question the validity of volumetric ratios as useful measures of information-processing capacity and the justification for the near-exclusive focus of comparative studies on the neocortex.

    “These results question both the validity of volumetric ratios as useful measures of information-processing capacity and the justification based on their variability across species for the near-exclusive focus of comparative studies on the neocortex.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § 5. Cognitive implications

    The cerebellum has a broader role than previously recognized, including emotion, non-motor associative learning, working memory and mental rehearsal, verbal working memory and other language functions, spatial and episodic memory, event prediction, empathy and predicting others' actions, imitation, planning and decision-making, individual variation in cognitive performance, and cognitive-developm

    “However, in the past 10 years or so considerable evidence has accumulated that the cerebellum has a broader role than previously recognized, including emotion [75,76], non-motor associative learning [77], working memory and mental rehearsal [77,78], verbal working memory and other language functions [76,78–81], spatial and episodic memory [79,81,82], event prediction [83], empathy and predicting”
    Quote in the paperSubstantial claim0 of 7 sources checked
    • cites [75] Colibazzi T., et al. 2010. Neural systems subserving valence and arousal during the experience of induced emotions. Emotion 10, 377–389 10.1037/a0018484 (doi:10.1037/a0018484) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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      Not checked in the free run.

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      Not checked in the free run.

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      Not checked in the free run.

    • cites [81] Leggio M. G., Chiricozzi F. R., Clausi S., Tedesco A. M., Molinari M. 2011. The neuropsychological profile of cerebellar damage: the sequencing hypothesis. Cortex 47, 137–144 10.1016/j.cortex.2009.08.011 (doi:10.1016/j.cortex.2009.08.011) [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 2. Methods

    After taking scaling against other brain structures into account, primates have relatively large neocortices and a relatively high density of cortical neurons.

    “After taking scaling against other brain structures into account, primates have relatively large neocortices [23], and a relatively high density of cortical neurons [48].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [23] Barton R. A., Harvey P. H. 2000. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058 10.1038/35016580 (doi:10.1038/35016580) [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [48] Barton R. A. 2006. Primate brain evolution: integrating comparative, neurophysiological and ethological data. Evol. Anthrop. 15, 224–236 10.1002/evan.20105 (doi:10.1002/evan.20105) [DOI] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 11. Conclusions

    Motor control and hierarchical action planning systems were secondarily adapted for syntax.

    “These proposals agree with Sterelny's [114] scenario for language evolution which suggests that the control of motor sequences involved in ape foraging skills provided a cognitive platform for gestural communication and thence ultimately syntax and language, and with Fitch's [101] proposal that motor control and hierarchical action planning systems were secondarily adapted for syntax.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [101] Fitch W. T. 2011. The evolution of syntax: an exaptationist perspective. Front. Evol. Neurosci. 3, 9 10.3389/fnevo.2011.00009 (doi:10.3389/fnevo.2011.00009) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 11. Conclusions

    The control of motor sequences involved in ape foraging skills provided a cognitive platform for gestural communication and thence ultimately syntax and language.

    “These proposals agree with Sterelny's [114] scenario for language evolution which suggests that the control of motor sequences involved in ape foraging skills provided a cognitive platform for gestural communication and thence ultimately syntax and language, and with Fitch's [101] proposal that motor control and hierarchical action planning systems were secondarily adapted for syntax.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [114] Sterelny K. 2012. Language, gesture, skill: the coevolutionary foundations of language. Phil. Trans. R. Soc. B 367, 2141–2151 10.1098/rstb.2012.0116 (doi:10.1098/rstb.2012.0116) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation
    § 11. Conclusions

    The proposals in this paper agree with Sterelny's scenario for language evolution and with Fitch's proposal that motor control and hierarchical action planning systems were secondarily adapted for syntax.

    “These proposals agree with Sterelny's [114] scenario for language evolution which suggests that the control of motor sequences involved in ape foraging skills provided a cognitive platform for gestural communication and thence ultimately syntax and language, and with Fitch's [101] proposal that motor control and hierarchical action planning systems were secondarily adapted for syntax.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [114] Sterelny K. 2012. Language, gesture, skill: the coevolutionary foundations of language. Phil. Trans. R. Soc. B 367, 2141–2151 10.1098/rstb.2012.0116 (doi:10.1098/rstb.2012.0116) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [101] Fitch W. T. 2011. The evolution of syntax: an exaptationist perspective. Front. Evol. Neurosci. 3, 9 10.3389/fnevo.2011.00009 (doi:10.3389/fnevo.2011.00009) [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

20 of 20

  • The paper relies on this without support.

    The comparative brain and behavioural data used are representative of species' typical cognitive abilities and evolutionary history.

    “I use phylogenetic comparative analyses of brain component volumes and neuron numbers to test hypotheses about the evolutionary determinants and cognitive consequences of brain structure evolution.”

  • The paper relies on this without support.

    The cerebellum's role in cognitive functions in modern species reflects its role in evolutionary history.

    “The confluence of these comparative patterns, studies of ape foraging skills and social learning, and recent evidence on the cognitive neuroscience of the cerebellum, suggest an important role for the cerebellum in the evolution of the capacity for planning, execution and understanding of complex behavioural sequences—including tool use and language.”

  • The paper relies on this without support.

    The behavioural variables (extractive foraging, tool use, social group size) are valid measures of the cognitive demands they are taken to represent.

    “A new phylogenetic comparative analysis controlling for allometric effects supports this contention (table 1).”

  • The paper relies on this without support.

    Different selection pressures have acted on different neural systems at different times.

    “because different selection pressures have acted on different neural systems at different times.”

  • The paper relies on this without support.

    There are so many neurons in the cerebellum.

    “Any account of human neuro-cognitive evolution needs to explain why there are so many neurons in the cerebellum.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The foraging hypothesis posits that dietary complexity, indexed by field reports of dietary breadth and reliance on fruit, was the primary driver of primate cognitive evolution.

    “The foraging hypothesis posits that dietary complexity, indexed by field reports of dietary breadth and reliance on fruit (a spatiotemporally distributed resource), was the primary driver of primate cognitive evolution (151-154).”

    From The evolution of self-control. (2014) · cites this paper as [153]

  • These trends are further extended in humans with an additional investment in absolute brain size.

    “These trends are further extended in humans with an additional investment in absolute brain size (see figure 1c and electronic supplementary material, S2) [63].”

    From Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution (2013) · cites this paper as [63]

Cites

Flagged first, then by citations

Research works printed but not linked: 6

  1. Stephan H., 1991, Comparative brain research in mammals, vol. 1. Insectivores
  2. Brodmann K., 1912, Neue Ergebnisse uber die vergleichende histologische Lokalisation der Grosshirnrinde mit besonderer Berücksichtigung des Stirnhirns Anat, Anzeiger, 41, 157
  3. 10.1098/rstb.2006.2001 · DOI · Paper page
  4. Barton R. A., Human frontal lobes are not disproportionately expanded, Nat. Neurosci.
  5. Byrne R. W., 2006, The roots of human sociality, 478
  6. Gibson K. R., 1986, Cognition, brain size and the extraction of embedded food resources, Primate ontogeny, cognition and social behaviour, 93

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Authors
Barton, R. A.
Affiliations
Durham University (GB)
Corresponding author
Barton, Robert A.
ORCID
Barton, Robert A.
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2012-08-05
Volume
367
Issue
1599
Pages
2097-2107
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2012.0112
PMC
PMC3385677
OpenAlex
W2158848857
Semantic Scholar
0737e5159ac418bf02a2257cdeae8c6d386bcbe8
Cited by
210
References
133
Citations by year
2026: 6 · 2025: 7 · 2024: 15 · 2023: 11 · 2022: 16 · 2021: 24 · 2020: 18 · 2019: 12 · 2018: 12 · 2017: 21 · 2016: 20 · 2015: 10 · 2014: 18 · 2013: 11 · 2012: 7
FWCI
22.13
Type
journal article
Language
en
Open access
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Durham Research Online (Durham University) (acceptedVersion)
  • Durham Research Online (Durham University) (acceptedVersion, other-oa)
  • Durham Research Online (Durham University) (submittedVersion, cc-by)
Topics
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Embodied and Extended Cognition
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords
cerebellum, cognitive evolution, neocortex, brain evolution, correlated evolution, apes, social learning, tool use, language, embodied cognition, executive function, behavioral sequences
MeSH terms
Animals, Cerebellum, Cognition, Biological Evolution, Humans, Language, Neurons, Organ Size, Phylogeny, Species Specificity, Computational Biology, Neocortex, Tool Use Behavior, Emotional Intelligence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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