Robert Barton Evolutionary Anthropology Research Group, Durham University, UK
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Transcript of Robert Barton Evolutionary Anthropology Research Group, Durham University, UK
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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)
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* 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