Cinderella
of the brain:
Cerebellar
involvement
in brain
the under-appreciated
roles of the cerebellum
evolution, development
and in
cognitive evolution, development and pathology
behaviour
Robert Barton
Evolutionary Anthropology Research Group,
Durham University, UK
EARG
1
Cerebella comes to the ball…
Wikipedia: ‘Cinderella’ - one whose attributes were unrecognized, or
one who unexpectedly achieves recognition… after a period of
obscurity and neglect
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
Talk structure
I. Rethinking the brain: an evolutionary
approach
I. Convergent evidence from evolution and
cognitive neuroscience
- The role of the cerebellum
II. Links between evolution, development and
developmental disruption
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
4
A Victorian view of the brain?
Parvizi (2011) Social neuroscience iFirst, 1–6
“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).”
5
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.”6
“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”
7
“Organs of extreme perfection &
complication”
8
But….
9
A cornucopia of theories
10
A
A?
B
11
Anthropocentric evolutionary teleology
“research is beginning to pin down genes that evolved
rapidly during the transition from chimps to people”
12
chimpanzee
?
Common
ancestor
human
7 million years
13
How to avoid
Just-so
stories:
phylogenetic
comparative
analysis
Common
ancestor
Millions of years
14
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”)
15
Is the neocortex the “intelligent” bit of
the brain?
The structure that expanded most
and that correlates with intelligent
behaviour across species:
• “the crowning achievement of
evolution and the biological
substrate of human mental
prowess” (Rakic 2009)
Cortical ballooning
87%
80%
70-75%
14%
Proportional
size
73%
Body size and % cortex are positively
correlated (p<0.0001)
Bigger cortex = more white
matter…
grey
white
Cerebellum
Cortex
0.5
0.45
0.4
Proportion0.35
0.3
devoted to0.25
white 0.2
matter 0.15
0.35
0.1
0.1
0.3
0.25
0.2
0.15
-1
0.05
-0.5
0
0.5
1
1.5
0
-10
10
30
50
70
90
Cortex volume
110
130
150
Cerebellum volume
2
2.5
…and lower neuron density
Cerebellum
Cortex
Slope =-0.28
Evolutionary
change in
neuron
density
Slope = -0.08
Evolutionary change in brain volume
19
Volumetric ratios do not correspond to
numbers of neurons:
Volume proportions
cerebellum
neocortex
Neuron number proportions
No correlation between N/C volume ratio and N/C neuron ratio:
(r2=0.1, p=0.27)
20
Relative number
of neurons
Relative
size of cerebellum
16 billion neurons
70 billion neurons
Glickstein (1993): “What on earth
do (all these neurons) do?”
21
Primate brain size: neocortex, but
cerebellum too:
insectivores
lemurs
anthropoids
primates
22
resid(m1)
-0.5
neocortex
0.0
0.5
1.0
Connected structures evolve
together…
-0.3
-0.2
-0.1
0.0
0.1
diencephalon
1.0
resid(m3)
0.5
Rel cereb
-0.5
resid(m1)
0.0
neocortex
-0.4
-0.2
0.0
0.2
resid(m2)
cerebellum
0.4
0.6
Diagram adapted from Boso et al.
0.2
0.3
Cortical and cerebellar expansion
primates
non-primates
Cortex
Cerebellum
neocortex
Log neurons in rest of brain
Log neurons in rest of brain
Log N of
neurons
24
Correlated evolution of neuron numbers
resid(m1)
relative
number of
cortical
neurons
0.5
1.0
Controlling for neurons in other brain areas :
Multiple PGLS: p<0.0001
-0.5
0.0
(Data from HerculanoHouzel)
-0.6
-0.4
-0.2
0.0
0.2
0.4
0.6
resid(m2)
relative number of
cerebellar neurons
0.8
Anatomy predicts evolution
Anatomy
Evolution
0.0
-0.5
cerebellum
-1.0
pons
Relative
size of
neocortex
resid(m3)
thalamus
0.5
1.0
neocortex
-0.4
-0.2
0.0
0.2
0.4
Relative size of
cerebellum
0.6
resid(m4)
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
BUT…apes are different
Cerebellum volume
1: p= 0.0003
4: p<0.05
Phylogenetic ANCOVA: p=0.00015
2: p=0.0003
5: p=0.03
3.
3.
6: p>0.05
Neocortex volume
Barton & Venditti, Current Biology, in press
The Great ape leap forward:
explosive evolution of the cerebellum
cerebellum
neocortex
Bayesian estimation of rates of volumetric evolution
Barton & Venditti, Current Biology in press
Phylogenetic ANCOVA:
p=0.000609
Great ape technical intelligence
-Extractive foraging, tool use
-Fine sensory-motor control
-Byrne: iterated, multi-stage
algorithms to solve
“syntactical” problems
R. Byrne
-The origin of syntax?
(cerebellar role in verbal
fluency etc)
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Evolution of brain and behaviour in
primates
Group size
Cerebellum
Neocortex
32.64, p=0.012
4.55, p=0.0006
Controlling for size of other brain structures
Barton (2012) Phil. Trans Roy. Soc.
Extractive foraging
3.58, p=0.0009
2.07, p=0.044
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:
Capacity to perceive, model, empathize with and
anticipate the behaviour of others
“computational elements
developed for
sensorimotor control are
effective in inferring the
mental states of others”
(Oztop et al 2005)
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
Boldue t al. (2012) Cerebellum 11:531–542
• Language
Kana et al. (2011) Neurosci Biobehav Rev 35 894–902
• IQ
Murdoch (2010) Cortex 46 858– 868
Hogan et al. (2011) Cortex 47 44 – 450
• Early deprivation
Bauer et al Biol. Psych. (2009) 66:1100–1106
• Cerebellar Cognitive
Schmahmann & Sherman (1998) Brain 121, 561–579
Affective Syndrome
A non-controversy
= Cognitive?
= Catholic?
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
Prenatal growth
(monkey)
Cortex
Cerebellum
Diencephalon
Midbrain
Medulla
birth
Data from DeVito et al (1994)
Variation in size
across species
correlates with
gestation length
Postnatal development
macaque
Human cerebellar growth
60
120
110
volume
20
6
*
100
90
4
80
70
2
60
0
100
200
birth
Data from DeVito et al (1994)
2
4
6
8
10
12
14
postnatal years
300
* Variation in adult size
correlates with weaning age
Data from Wu et al. (2011) Pediatric Research 69, 80-83
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”
Granule cells
in cerebellar
hemispheres
Age in months
12
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
Acknowledgements
• Chris Venditti
• Isabella Capellini
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