Robert Barton Evolutionary Anthropology Research Group, Durham University, UK

1. Cinderella of the brain: the under-appreciated roles of the cerebellum in cognitive evolution, development and pathology Cerebellar involvement in brain evolution, development and behaviour Robert Barton Evolutionary Anthropology Research Group, Durham University, UK EARG

2. 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

3. Talk structure • Rethinking the brain: an evolutionary approach • Convergent evidence from evolution and cognitive neuroscience - The role of the cerebellum • Links between evolution, development and developmental disruption

4. 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

5. 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).”

6. Inhibition (& disinhibition) Parvizi (2011) Social Neuroscience iFirst, 1–6 the brain is hierarchically organized into higher cortical and lower subcortical structures; the higher structures, with the frontal lobes being the highest, have expanded disproportionately …the lower structures are primitive the higher structures are involved in human cognitive faculties such as thinking, whereas the lower structures are engaged in instinctual and innate behavior the higher brain structures constrain and inhibit the lower structures; when such inhibition fails, the lower structures are “released” to act in their innate way and against the social norms of appropriateness.”

7. “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”

8. “Organs of extreme perfection & complication”

9. But….

10. A cornucopia of theories

11. A A? B

12. Anthropocentric evolutionary teleology “research is beginning to pin down genes that evolved rapidly during the transition from chimps to people”

13. chimpanzee ? Common ancestor human 7 million years

14. How to avoid Just-so stories: phylogenetic comparative analysis Common ancestor Millions of years

15. 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”)

16. Is the neocortexthe “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)

17. Cortical ballooning 87% 80% 73% 70-75% 14% Body size and % cortex are positively correlated (p<0.0001) Proportional size

18. Bigger cortex = more white matter… grey white Cerebellum Cortex Proportion devoted to white matter Cortex volume Cerebellum volume

19. …and lower neuron density Cerebellum Cortex Slope =-0.28 Slope = -0.08 Evolutionary change in neuron density Evolutionary change in brain volume

20. Volumetric ratios do not correspond to numbers of neurons: cerebellum neocortex Volume proportions Neuron number proportions No correlation between N/C volume ratio and N/C neuron ratio: (r2=0.1, p=0.27)

21. Relative size of cerebellum Relative number of neurons 16 billion neurons 70 billion neurons Glickstein (1993): “What on earth do (all these neurons) do?”

22. Primate brain size: neocortex, but cerebellum too: insectivores lemurs primates anthropoids

23. Connected structures evolve together… neocortex diencephalon Relcereb neocortex Diagram adapted from Boso et al. 2010 cerebellum

24. Cortical and cerebellar expansion primates non-primates Cerebellum Cortex neocortex Log N of neurons Log neurons in rest of brain Log neurons in rest of brain

25. Correlated evolution of neuron numbers Controlling for neurons in other brain areas : relative number of cortical neurons Multiple PGLS: p<0.0001 (Data from Herculano-Houzel) relative number of cerebellar neurons

26. Anatomy predicts evolution Anatomy Evolution neocortex thalamus Relative size of neocortex pons cerebellum Relative size of cerebellum Barton (2012) Whiting & Barton (2003)

27. 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

28. 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

29. Cortico-cerebellar adaptive control systems Ramnani (2006) NATURE REVIEWS | NEUROSCIENCE

30. BUT…apes are different 4: p<0.05 1: p= 0.0003 Phylogenetic ANCOVA: p=0.00015 2: p=0.0003 5: p=0.03 Cerebellum volume 3. 6: p>0.05 3. Neocortex volume Barton & Venditti, Current Biology, in press

31. The Great ape leap forward: explosive evolution of the cerebellum cerebellum neocortex Bayesian estimation of rates of volumetric evolution Phylogenetic ANCOVA: p=0.000609 Barton & Venditti, Current Biology in press

32. Great ape technical intelligence • 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) R. Byrne

33. Evolution of brain and behaviour in primates 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 Controlling for size of other brain structures Barton (2012) Phil. Trans Roy. Soc.

34. Secondary adaptation of technical for social intelligence? “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) Photo: R. Byrne

35. Social learning &metacognition • Linkages between neural systems for: • - performing actions • social perception & understanding of actions • “Mirror neurons” Drawing by Amy Whiten

36. “Embodied simulation” & empathy: Capacity to perceive, model, empathizewith 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)

37. 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

38. 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

39. 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 11:531–542 Kana et al. (2011) NeurosciBiobehav Rev 35 894–902 Murdoch (2010) Cortex46 858– 868 Hogan et al. (2011) Cortex 47 44 – 450 Bauer et al Biol. Psych. (2009) 66:1100–1106 Schmahmann & Sherman (1998) Brain 121, 561–579

40. A non-controversy = Cognitive? = Catholic?

41. 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)

42. “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)

43. Part III: Links between evolution, development & pathology Prenatal growth (monkey) Cortex Variation in size across species correlates withgestation length Cerebellum Diencephalon Medulla Midbrain birth Data from DeVito et al (1994)

44. Postnatal development macaque 60 Human cerebellar growth 20 6 * Cerebellum volume 4 2 postnatal years 100 200 300 * Variation in adult size correlates with weaning age birth Data from DeVito et al (1994) Data from Wu et al. (2011) Pediatric Research 69, 80-83

45. 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 12 Age in months

46. The importance of play Social play Non-social play Frequencies Montgomery (2014) Animal Behaviour 90, 281-290

47. 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

48. Acknowledgements • Chris Venditti • Isabella Capellini