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Robert BartonEvolutionary Anthropology Research Group,

Durham University, UK

EARG

Cerebellar involvement in brain evolution, development and

behaviour

Cinderella of the brain: the under-appreciated roles of the cerebellum in cognitive evolution, development and pathology

Cerebella comes to the ball…

a relatively small structure at the bottom of the brain that seems to hide under the occipital lobes as if unwilling to assume a more prominent position… “ Beaton & Marien (2010) Cortex 46

Wikipedia: ‘Cinderella’ - one whose attributes were unrecognized, or one who unexpectedly achieves recognition… after a period of obscurity and neglect

Talk structure

I. Rethinking the brain: an evolutionary approach

II. Convergent evidence from evolution and cognitive neuroscience

- The role of the cerebellum

III. Links between evolution, development and developmental disruption

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What we thought we knew about brain evolution

• The cortex is the interesting bit– Expanded more than other areas– Responsible for higher cognitive processes– Controls instinctive reactions (inhibition)– Seat of rationality

• Especially frontal regions (prefrontal cortex)

• Areas at the back of the brain (primary sensory cortices, cerebellum) are primitive and conserved – not involved in brain expansion or cognitive evolution

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“the higher nervous arrangements evolved out of the lower to keep down those lower, just as a government evolved out of a nation controls as well as directs that nation

(Hughlings-Jackson, 1884).”

Parvizi (2011) Social neuroscience iFirst, 1–6

A Victorian view of the brain?

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Inhibition (& disinhibition)Parvizi (2011) Social Neuroscience iFirst, 1–6 1. the brain is hierarchically organized into higher

cortical and lower subcortical structures;

2. the higher structures, with the frontal lobes being the highest, have expanded disproportionately …the lower structures are primitive

3. the higher structures are involved in human cognitive faculties such as thinking, whereas the lower structures are engaged in instinctual and innate behavior

4. the higher brain structures constrain and inhibit the lower structures;

5. when such inhibition fails, the lower structures are “released” to act in their innate way and against the social norms of appropriateness.”

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“The main problem with corticocentrism is the lack of appreciation of the reciprocal connectivity between cortical and subcortical structures. The problem is to see the relationship between cortical and subcortical structures in a one-way linear manner, and almost always in a top-down and hierarchical manner”

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“Organs of extreme perfection & complication”

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But….

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A cornucopia of theories

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A

B

A?

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Anthropocentric evolutionary teleology

“research is beginning to pin down genes that evolved rapidly during the transition from chimps

to people”

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7 million years

Common ancestor

?

chimpanzee

human

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Commonancestor

Millions of years

How to avoid Just-so stories:

phylogenetic comparative

analysis

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Part II: Neuro-cognitive evolution and the emerging role of the cerebellum

Studying how the evolution of brains (size, structure, numbers of neurons) and cognition relate – ~15 years

Data parasitism (or “scientific necrophilia”)

Is the neocortex the “intelligent” bit of the brain?

• “the crowning achievement of evolution and the biological substrate of human mental prowess” (Rakic 2009)

The structure that expanded most and that correlates with intelligent behaviour across species:

Cortical ballooning

80%

87%

73%

14%

70-75%

Proportional size

Body size and % cortex are positively correlated (p<0.0001)

Bigger cortex = more white matter…

-10 10 30 50 70 90 110 130 1500

0.05

0.1

0.15

0.2

0.25

0.3

0.35

0.4

0.45

0.5

Proportion devoted to

white matter

Cortex volume

-1 -0.5 0 0.5 1 1.5 2 2.50.1

0.15

0.2

0.25

0.3

0.35

Cerebellum volume

Cortex Cerebellum

white

grey

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Evolutionary change in

neuron density

Evolutionary change in brain volume

Cortex Cerebellum

…and lower neuron density

Slope =-0.28 Slope = -0.08

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Volumetric ratios do not correspond to numbers of neurons:

No correlation between N/C volume ratio and N/C neuron ratio:(r2=0.1, p=0.27)

Volume proportions Neuron number proportions

cerebellumneocortex

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Glickstein (1993): “What on earth do (all these neurons) do?”

Relative size of cerebellumRelative number of neurons

16 billion neurons

70 billion neurons

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insectivores

lemursanthropoids

primates

Primate brain size: neocortex, but cerebellum too:

Rel cereb

neocortex

diencephalon

neocortex

cerebellum Diagram adapted from Boso et al. 2010

Connected structures evolve together…

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neocortex

Log neurons in rest of brain

Cortex Cerebellum

Log N of neurons

Log neurons in rest of brain

primatesnon-primates

Cortical and cerebellar expansion

Correlated evolution of neuron numbers

relative number of

cortical neurons

relative number of cerebellar neurons

Multiple PGLS: p<0.0001

(Data from Herculano-Houzel)

Controlling for neurons in other brain areas :

ponscerebellum

neocortex

thalamus

Anatomy

Anatomy predicts evolution

Relative size of

neocortex

Relative size of cerebellum

Evolution

Barton (2012)Whiting & Barton (2003)

Cortical regions with reciprocal cerebellar connections

Parietal Visually guided hand movements; Motor planning; Verbal processing and storage; Spatial navigation

Temporal Articulatory aspects of language

Frontal/prefrontal Language; working memory;directed attention; planning

Occipital cortex Vision/visuo-motor

Cortico-cerebellar function (broadly)

• Adaptive control (cognitive and supposedly non-cognitive processes share overlapping neural substrates and common computational architectures)

– ‘Sensory-motor’

– ‘Cognitive’: learning, planning, working memory & mental rehearsal, verbal fluency & other language functions, episodic memory, event prediction, empathy, imitation

– Planning and comprehension of complex sequences of behaviour

Cortico-cerebellar adaptive control systems

Ramnani (2006) NATURE REVIEWS | NEUROSCIENCE

2: p=0.0003

3.

1: p= 0.0003

Barton & Venditti, Current Biology, in press

4: p<0.05

Phylogenetic ANCOVA: p=0.00015

BUT…apes are different

Neocortex volume

Cere

bellu

m v

olum

e

6: p>0.05

5: p=0.03

3.

The Great ape leap forward: explosive evolution of the cerebellum

Barton & Venditti, Current Biology in press

Phylogenetic ANCOVA: p=0.000609

Bayesian estimation of rates of volumetric evolution

cerebellum

neocortex

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Great ape technical intelligence

R. Byrne

-Extractive foraging, tool use

-Fine sensory-motor control

-Byrne: iterated, multi-stage algorithms to solve “syntactical” problems

-The origin of syntax? (cerebellar role in verbal fluency etc)

Group size Extractive foraging

Cerebellum 32.64, p=0.012 3.58, p=0.0009

Neocortex 4.55, p=0.0006 2.07, p=0.044

Evolution of brain and behaviour in primates

Controlling for size of other brain structures

Barton (2012) Phil. Trans Roy. Soc.

Secondary adaptation of technical for social intelligence?

Photo: R. Byrne

“The ability of great apes to learn new manual routines by parsing action components may have driven their qualitatively greater social skill, suggesting that strict partition of physical and social cognition is likely to be misleading” (Byrne & Bates 2010)

Social learning & metacognition

Linkages between neural systems for:

- performing actions

- social perception & understanding of actions

“Mirror neurons”

Drawing by Amy Whiten

“Embodied simulation” & empathy:

“computational elements developed for

sensorimotor control are effective in inferring the mental states of others”

(Oztop et al 2005)

Capacity to perceive, model, empathize with and anticipate the behaviour of others

Where did language come from?

• Pinker: language is an adaptation – Module that has no precursor in non-

human species, an adaptation for communication via syntax

• Gould: language is an exaptation – by-product of a large brain

Language as sensory-motor control

• Neurobiology now implicates the cerebellum– Fits with the idea that the cerebellum manages complex sequences

• “Language” and “motor” brain areas overlap: Broca’s area is activated by skilled motor tasks such as tool-making

• Confluence of data on brain evolution and cognitive neuroscience suggests language a ‘secondary adaptation’ built on sensory-motor control processes adapted for syntactical processing

• Neither Gould’s exaptation nor Pinker’s module

Evidence for cerebellar cognition• Non-motor associative learning• Cognitive sequencing• Spatial cognition• Working memory• Event prediction• Language

Individual variation correlates with cerebellar size/structure:• Autism• Global development score• Language• IQ• Early deprivation• Cerebellar Cognitive

Affective Syndrome

Boldue t al. (2012) Cerebellum 11:531–542Kana et al. (2011) Neurosci Biobehav Rev 35 894–902Murdoch (2010) Cortex 46 858– 868Hogan et al. (2011) Cortex 47 44 – 450Bauer et al Biol. Psych. (2009) 66:1100–1106Schmahmann & Sherman (1998) Brain 121, 561–579

A non-controversy

= Catholic?

= Cognitive?

Embodied cognitive evolution

• Sensory-motor and ‘cognitive’ processes – and their evolution - are not separate

• Cognitive evolution to be understood as the elaboration of specialized systems for embodied adaptive control (not increasing top-down control by some kind of central executive)

“Thinking as internalized movement…

“…a reconstruction of possible movements and their possible consequences becomes, in fact, the substrate of ‘thinking’”

Rodolfo Llinás (in Mindwaves, 1987)

Part III: Links between evolution, development & pathology

Cortex

CerebellumDiencephalon

Medulla

birthData from DeVito et al (1994)

Prenatal growth (monkey)

Variation in size across species correlates with

gestation length

Midbrain

Postnatal development

100 200 300

2

4

620

60

Cerebellum

volu

me

birth

0 2 4 6 8 10 12 1460

70

80

90

100

110

120

postnatal years

macaque Human cerebellar growth

Data from Wu et al. (2011) Pediatric Research 69, 80-83Data from DeVito et al (1994)

*

* Variation in adult size correlates with weaning age

85% of human cerebellar granule cells produced post-natally

• Kiessling et al (2014) “the human cerebellum has a much higher functional plasticity during the first year of life than previously thought, and may respond very sensitively to internal and external influences during this time…important implications for several neuropsychiatric conditions”

Age in months12

Granule cells in cerebellar hemispheres

The importance of play

Social play Non-social play

Frequencies

Montgomery (2014) Animal Behaviour 90, 281-290

Conclusion• Like Sally Goddard-Blythe says – don’t divorce the

mind from the body (and sensory-motor control)

• Human cognitive evolution and development are embodied

• The cerebellum plays a key role – it is a new frontier for studying cognitive evolution, development and developmental vulnerabilities

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Acknowledgements

• Chris Venditti• Isabella Capellini