Abstract
Until recently, few studies have focused on the evolution of the cerebellum in human lineage. While the major functional role of the cerebellum was traditionally thought to be fine motor control, recent neuroimaging and neurological evidence suggests that the cerebellum is deeply involved in a variety of cognitive and social functions. Moreover, the cerebellum has been found to have a unique gross anatomy and microstructure. In contrast to the cerebrum, the cortex of the cerebellum is structured as a homogeneous sheet with a similar internal structure throughout. This cortex contains cerebellar neural circuitry that functions as a learning system capable of constructing and storing internal models of the external environment. Converging evidence suggests that the greater the volume of the cerebellar cortex, the more internal models it is able to store. This neuroanatomical organization may affect innate learning, cognitive ability, and the human capacity to innovate. In this chapter, we review the relationship between cerebellar volume and various cognitive abilities in modern humans and then discuss the evolutionary changes of cerebellar size based on the comparative anatomy of extant primates and the evidence from fossil specimens with our recent findings.
References
Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61
Allen JS, Damasio H, Grabowski TJ (2002) Normal neuroanatomical variation in the human brain: an MRI-volumetric study. Am J Phys Anthropol 118:341–358
Amano H, Kikuchi T, Morita Y, Kondo O, Suzuki H, Ponce de León MS, Zollikofer CPE, Bastir M, Stringer C, Ogihara N (2015) Virtual reconstruction of the Neanderthal Amud 1 cranium. Am J Phys Anthropol 158:185–197
Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6:297–311
Ashburner J, Friston KJ (2000) Voxel-based morphometry: the methods. NeuroImage 11:805–821
Baddeley A (1992) Working memory. Science 255:556–559
Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829–839
Baddeley AD, Hitch G (1974) Working memory. In: Bower G (ed) Psychology of learning and motivation volume 8. Academic Press, New York, pp 47–89
Baier B, Müller NG, Dieterich M (2014) What part of the cerebellum contributes to a visuospatial working memory task? Ann Neourol 76:754–757
Baillieux H, De Smet HJ, Lesage G, Paquier P, De Deyn PP, Mariën P (2006) Neurobehavioral alterations in an adolescent following posterior fossa tumor resection. Cerebellum 5:289–295
Barkley RA (2001) The executive functions and self-regulation: an evolutionary neuropsychological perspective. Neuropsychol Rev 11:1–29
Barton RA, Venditti C (2014) Rapid evolution of the cerebellum in humans and other great apes. Curr Biol 24:2440–2444
Bostan AC, Dum RP, Strick PL (2013) Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci 17:241–254
Braitenberg V, Atwood RP (1958) Morphological observations on the cerebellar cortex. J Comp Neurol 109:1–33
Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC (1997) A parametric study of prefrontal cortex involvement in human working memory. NeuroImage 5:49–62
Broadfield DC, Holloway RL, Mowbray K, Silvers A, Yuan MS, Màrquez S (2001) Endocast of Sambungmacan 3 (Sm 3): a new Homo Erectus from Indonesia. Anat Rec 262:369–379
Broom R, Schepers GWH (1946) The South African fossil Ape-man: the Australopithecinae. Transv Mus Mem 2:1–272
Broom R, Robinson JT, Schepers GWH (1950) Sterkfontein Ape-man Plesianthropus. Transv Mus Mem 4:1–117
Bruner E (2015) Functional craniology and brain evolution. In: Bruner E (ed) Human paleoneurology. Springer International Publishing, Cham, pp 57–94
Bruner E, Holloway RL (2010) A bivariate approach to the widening of the frontal lobes in the genus homo. J Hum Evol 58:138–146
Bruner E, Grimaud-Hervé D, Wu X, de la Cuétara JM, Holloway R (2015) A paleoneurological survey of Homo erectus endocranial metrics. Quat Int 368:80–87
Buckner RL (2013) The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80:807–815
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT (2011) The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106:2322–2345
Cantalupo C, Freeman H, Rodes W, Hopkins W (2008) Handedness for tool use correlates with cerebellar asymmetries in chimpanzees (Pan troglodytes). Behav Neurosci 122:191–198
Clark DA, Partha PM, Wang SSH (2001) Scalable architecture in mammalian brains. Nature 411:189–193
Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory task. Nature 386:604–608
Connolly CJ (1950) External morphology of the primate brain. Thomas, Springfield
Coolidge FL, Wynn T (2005) Working memory, its executive functions, and the emergence of modern thinking. Camb Archaeol J 15:5–26
D’Anastasio R, Wroe S, Tuniz C, Mancini L, Cesana DT, Dreossi D, Ravichandiran M, Attard M, Parr WC, Agur A, Capasso L (2013) Micro-biomechanics of the Kebara 2 hyoid and its implications for speech in Neanderthals. PLoS One 8:e82261
D’Esposito M, Detre JA, Alsop DC, Shin RK, Atlas S, Grossman M (1995) The neural basis of the central executive system of working memory. Nature 378:279–281
De Smet HJ, Paquier P, Verhoeven J, Mariën (2013) The cerebellum: its role in language and related cognitive and affective functions. Brain Lang 127:334–342
Dediu D, Levinson SC (2013) On the antiquity of language: the reinterpretation of Neandertal linguistic capacities and its consequences. Front Psychol 4:397
Desmond JE, Fiez JA (1998) Neuroimaging studies of the cerebellum: language, learning and memory. Trends Cogn Sci 2:355–362
Diedrichsen J (2006) A spatially unbiased atlas template of the human cerebellum. NeuroImage 33:127–138
E K-H, Chen S-HA, Ho M-HR, Desmond JE (2014) A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 35:593–615
Fabbro F, Moretti R, Bava A (2000) Language impairments in patients with cerebellar lesions. J Neurolinguistics 13:173–188
Falk D (2014) Interpreting sulci on hominin endocasts: old hypotheses and new findings. Front Hum Neurosci 8:134
Falk D, Clarke R (2007) New reconstruction of the Taung endocast. Am J Phys Anthropol 134:529–534
Fan L, Tang Y, Sun B, Gong G, Chen ZJ, Lin X, Yu T, Li Z, Evans AC, Liu S (2010) Sexual dimorphism and asymmetry in human cerebellum: an MRI-based morphometric study. Brain Res 1353:60–73
Fiez JA, Petersen SE, Cheney MK, Raichle ME (1992) Impaired non-motor learning and error detection associated with cerebellar damage: a single case study. Brain 115:155–178
Friede H (1981) Normal development and growth of the human neurocranium and cranial base. Scand J Plast Reconstr Surg Hand Surg 15:163–169
Frost JA, Binder JR, Springer JA, Hammeke TA, Bellgowan PSF, Rao SM, Cox RW (1999) Language processing is strongly left lateralized in both sexes: evidence from functional MRI. Brain 122:199–208
Grimaud-Hervé D (1997) L’évolution de l’encéphale chez l’Homo erectus et l’Homo sapiens. CNRS, Paris
Haier RJ, Jung RE, Yeo RA, Head K, Alkire MT (2004) Structural brain variation and general intelligence. NeuroImage 23:425–433
Hassid EI (1995) A case of language dysfunction associated with cerebellar infarction. Neurorehabil Neural Repair 9:157–160
Holloway RL, Yuan MS (2004) Endocranial morphology of AL 444-2. In: Kimbel WH, Rak Y, Johanson DC (eds) The skull of Australopithecus Afarensis. Oxford University Press, New York, pp 123–135
Holloway RL, Broadfield DC, Yuan MS (2004) The human fossil record, volume 3, brain endocasts: the paleoneurological evidence. Wiley-Liss, New York
Imamizu H, Kawato M (2009) Brain mechanisms for predictive control by switching internal models: implications for higher-order cognitive functions. Psychol Res 73:527–544
Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Puts B, Yoshioka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403:192–195
Ito M (1970) Neurophysiological basis of the cerebellar motor control system. Int J Neurol 7:162–176
Ito M (2008) Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9:304–313
Ito M (2011) The cerebellum: brain for an implicit self. FT Press, New Jersey
Jerison HJ (1973) Evolution of the brain and intelligence. Academic Press, New York
Jerison HJ (2006) Evolution of the frontal lobes. In: Miller BL, Cummings JL (eds) The human frontal lobes, second edition: functions and disorders. Gilford Press, New York, pp 107–118
Jissendi P, Baudry S, Balériaux D (2008) Diffusion tensor imaging (DTI) and tractography of the cerebellar projections to prefrontal and posterior parietal cortices: a study at 3T. J Neuroradiol 35:42–50
Justus TC, Ivry RB (2009) The cognitive neuropsychology of the cerebellum. Intern Rev Psychiatry 13:276–282
Kanai R, Rees G (2011) The structural basis of inter-individual differences in human behaviour and cognition. Nat Rev Neurosci 12:231–242
Kawato M, Furukawa K, Suzuki R (1987) A hierarchical neural-network model for control and learning of voluntary movement. Biol Cybern 57:169–185
Kelly RM, Strick PL (2003) Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 23:8432–8444
Keren-Happuch E, Chen SHA, Ho MHR, Desmond JE (2014) A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 35:593–615
Klein RG, Edgar B (2002) The dawn of human culture. Wiley, New York
Kobayashi Y, Matsui T, Haizuka Y, Ogihara N, Hirai N, Matsumura G (2014) Cerebral sulci and gyri observed on macaque endocasts. In: Akazawa T, Ogihara N, Tanabe HC, Terashima H (eds) Dynamics of learning in Neanderthals and modern humans, Cognitive and physical perspectives, vol 2. Springer, Tokyo, pp 131–137
Kochetkova VI (1978) Paleoneurology. VH Winston and Sons, Washington, DC
Kochiyama T, Tanabe HC, Ogihara N (2014) Reconstruction of the brain from skull fossil using computational anatomy. In: Akazawa T, Ogihara N, Tanabe HC, Terashima H (eds) Dynamics of learning in Neanderthals and modern humans, Cognitive and physical perspectives, vol 2. Springer, Tokyo, pp 191–200
Krause J, Lalueza-Fox C, Orlando L, Enard W, Burbano GRE, HA HJJ, Hänni C, Fortea J, de la Rasilla M, Bertranpetit J, Rosas A, Pääbo S (2007) The derived FOXP2 variant of modern humans was shared with Neandertals. Curr Biol 17:1908–1912
Krienen FM, Buckner RL (2009) Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex 19:2485–2497
Kubo D, Kono RT, Suwa G (2011) A micro-CT based study of the endocranial morphology of the Minatogawa I cranium. Anthropol Sci 119:123–135
Kubo D, Tanabe HC, Kondo O, Amano H, Yogi A, Murayama S, Ishida H, Ogihara N (2014a) Estimating the cerebral and cerebellar volumes of Neanderthals and Middle and Upper Paleolithic Homo sapiens. In: Akazawa T, Nishiaki Y (eds) RNMH Project Series No. 003: Abstracts of RNMH 2014 Second International Conference, pp 116–118
Kubo D, Tanabe HC, Kondo O, Ogihara N, Yogi A, Murayama S, Ishida H (2014b) Cerebellar size estimation from endocranial measurements: an evaluation based on MRI data. In: Akazawa T, Ogihara N, Tanabe HC, Terashima H (eds) Dynamics of learning in Neanderthals and modern humans, Cognitive and physical perspectives, vol 2. Springer, Tokyo, pp 209–215
Kyriacou A, Bruner E (2011) Brain evolution, innovation, and endocranial variations in fossil hominids. PaleoAnthropology 2011:130–143
Lange N, Froimowitz MP, Bigler ED, Lainhart JE (2010) Associations between IQ, total and regional brain volumes and demography in a large sample of healthy children and adolescents. Dev Neuropsychol 35:296–317
Leggio MG, Silveri MC, Petrosini L, Molinari M (2000) Phonological grouping is specifically affected in cerebellar patients: a verbal fluency study. J Neurol Neurosurg Psychiatry 69:102–106
Lieberman P (2009) The singing Neanderthals: the origins of music, language, mind and body, and: music, language, and the brain (review). Language 85:732–736
Lin WC, Chou KH, Chen HL, Huang CC, Lu CH, Li SH, Wang YL, Cheng YF, Lin CP, Chen CC (2012) Structural deficits in the emotion circuit and cerebellum are associated with depression, anxiety and cognitive dysfunction in methadone maintenance patients: a voxel-based morphometric study. Psychiatry Res 201:89–97
MacLeod C (2012) The missing link: evolution of the primate cerebellum. In: Hofman MA, Falk D (eds) Evolution of the primate brain: from neuron to behavior. Elsevier, Amsterdam, pp 165–187
MacLeod CE, Zilles K, Schleicher A, Rilling JK, Gibson KR (2003) Expansion of the neocerebellum in Hominoidea. J Hum Evol 44:401–429
Marr D (1969) A theory of cerebellar cortex. J Physiol Lond 202:437–470
Marvel CL, Desmond JE (2010) Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev 20:271–279
McDaniel MA (2005) Big-brained people are smarter: a meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence 33:337–346
Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292
Neubauer S, Gunz P, Weber GW, Hublin JJ (2012) Endocranial volume of Australopithecus africanus: new CT-based estimates and the effects of missing data and small sample size. J Hum Evol 62:498–510
O’Reilly JX, Beckmann CF, Tomassini V, Rammani N, Johansen-berg H (2009) Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex 20:953–965
Ogihara N, Amano H, Kikuchi T, Morita Y, Hasegawa K, Kochiyama T, Tanabe HC (2015) Towards digital reconstruction of fossil crania and brain morphology. Anthropol Sci 123:57–68
Paradiso S, Andreasen NC, O’Leary DS, Arndt S, Robinson RG (1997) Cerebellar size and cognition: correlations with IQ, verbal memory and motor dexterity. Neuropsychiar Neuropsychol Behav Neurol 10:1–8
Peña-Melian A (2000) Development of human brain. Hum Evol 15:99–112
Phillips KA, Hopkins WD (2007) Exploring the relationship between cerebellar asymmetry and handedness in chimpanzees (Pan troglodytes) and capuchins (Cebus apella). Neuropsychologia 45:2333–2339
Pliatsikas C, Johnstone T, Marinis T (2013) Grey matter volume in the cerebellum is related to the processing of grammatical rules in a second language: a structural voxel-based morphometry study. Cerebellum 13:55–63
Porrill J, Dean P, Anderson SR (2013) Adaptive filters and internal models: multivariate description of cerebellar function. Neural Netw 47:134–149
Pryor Pickering S (1930) Correlation of brain and head measurements, and relation of brain shape and size to shape and size of the head. Am J Phys Anthropol 15(1):1–52
Raz N, Gunning-Dixon F, Head D, Williamson A, Acker JD (2001) Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. Am J Neuroradiol 22:1161–1167
Rilling JK (2006) Human and nonhuman primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15:65–77
Rilling JK, Insel TR (1998) Evolution of the cerebellum in primates: differences in relative volume among monkeys, apes and humans. Brain Behav Evol 52:308–314
Schepers GWH (1950) The brain casts of the recently discovered Plesianthropus skulls. Transv Mus Mem 2:89–117
Schmahmann JD (1996) From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp 4:174–198
Schmahmann JD (2004) Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuro-Oncol 16:367–378
Schmahmann JD, Sherman JC (1998) The cerebellar cognitive affective syndrome. Brain 121:561–579
Semendeferi K, Damasio H (2000) The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. J Hum Evol 38:317–332
Silveri MC, Leggio MG, Molinari M (1994) The cerebellum contributes to linguistic production: a case of agrammatic speech following a right cerebellar lesion. Neurology 44:2047–2050
Smaers JB, Steele J, Case CR, Amunts K (2013) Laterality and the evolution of the prefronto-cerebellar system in anthropoids. Ann N Y Acad Sci 1288:59–69
Snyder PJ, Bilder RM, Wu H, Bogerts B, Lieberman JA (1995) Cerebellar volume asymmetries are related to handedness: a quantitative MRI study. Neuropsychologia 33:407–419
Sousa AA d, Proulx MJ (2014) What can volumes reveal about human brain evolution? A framework for bridging behavioral, histometric, and volumetric perspectives. Front Neuroanat 8:51
Szeszko PR, Gunning-Dixon F, Ashtari M, Snyder PJ, Lieberman JA, Bilder RM (2003) Reversed cerebellar asymmetry in men with first-episode schizophrenia. Biol Psychiatry 53:450–459
Van Overwalle F, Mariën P (2016) Functional connectivity between the cerebrum and cerebellum in social cognition: a meta-study analysis. NeuroImage 124:248–255
Weaver AGH (2001) The cerebellum and cognitive evolution in Pliocene and Pleistocene hominids. Dissertation, University of New Mexico
Weaver AH (2005) Reciprocal evolution of the cerebellum and neocortex in fossil humans. Proc Natl Acad Sci U S A 102:3576–3580
Weil A (1929) Measurements of cerebral and cerebellar surfaces: comparative studies of the surfaces of endocranial casts of man, prehistoric men, and anthropoid apes. Am J Phys Anthropol 13:69–90
White DD (2005) Size and shape of the cerebellum in Catarrhine primates and Plio-Pleistocene fossil hominins: a paleoneurological analysis of endocranial casts. Dissertation, State University of New York
Whiting BA, Barton RA (2003) The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J Hum Evol 44:3–10
Wolpert DM, Kawato M (1998) Multiple paired forward and inverse models for motor control. Neural Netw 11:1317–1329
Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347
Wynn T, Coolidge FL (2003) The role of working memory in the evolution of managed foraging. Before Farming 2003(2):1–16
Yeo BTT, Sabuncu MR, Vercauteren T, Holt DJ, Amunts K, Zilles K, Golland P, Fischl B (2010) Learning task-optimal registration cost functions for localizing cytoarchitecture and function in the cerebral cortex. IEEE Trans Med Imaging 29:1424–1441
Yu F, Jiang Q-j, Sun X-y, Zhang R-w (2015) A new case of complete primary cerebellar agenesis: clinical and imaging findings in a living patient. Brain 138(6):e353–e353
Zettin M, Cappa SF, D’amico A, Rago R, Perino C, Perani D, Fazio F (1997) Agrammatic speech production after a right cerebellar haemorrhage. Neurocase 3:375–380
Acknowledgments
The authors would like to express the deepest gratitude to Prof. Takeru Akazawa of Kochi Institute of Technology for giving the opportunity to participate in the research project “Replacement of Neanderthals by Modern Humans: Testing Evolutionary Models of Learning” and for lending his continuous guidance and support throughout the course of the study. We’re also grateful to N. Sadato of the National Institute for Physiological Sciences, N. Ogihara of Keio University, O. Kondo of the University of Tokyo, and H. Ishida, A. Yogi, and S. Murayama of the University of the Ryukyus, for collaborations in this project. We also thank Y. Rak and I. Hershkovitz of Tel Aviv University and C. P. E. Zollikofer and M. Ponce de Leon of the University of Zurich for kindly allowing the use of CT scan data of the Amud 1 and Qafzeh 9; P. Mennecier and A. Froment of Muséum national d’Histoire naturelle for La Chappelle-aux-Saints 1, and Cro-Magnon 1; M. Bastir of Museo Nacional De Ciencias Naturales and C. Stringer of Natural History Museum for Forbes’ Quarry 1; and D. Lieberman, O. Herschensohn, and M. Morgan of Harvard University for Skhul 1. The CT scan data of the Mladec 1 were obtained from the digital archive of fossil hominoids, the University of Vienna. This project is supported by Scientific Research on Innovative Areas “Replacement of Neanderthals by Modern Humans: Testing Evolutionary Models of Learning” (#22101001, #22101006, #22101007) and “The Evolutionary Origin and Neural Basis of the Empathetic Systems” (#16H01486) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT), and by Grant-in-Aid for Scientific Research C#26350987.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Japan KK
About this chapter
Cite this chapter
Tanabe, H.C., Kubo, D., Hasegawa, K., Kochiyama, T., Kondo, O. (2018). Cerebellum: Anatomy, Physiology, Function, and Evolution. In: Bruner, E., Ogihara, N., Tanabe, H. (eds) Digital Endocasts. Replacement of Neanderthals by Modern Humans Series. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56582-6_18
Download citation
DOI: https://doi.org/10.1007/978-4-431-56582-6_18
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-56580-2
Online ISBN: 978-4-431-56582-6
eBook Packages: Social SciencesSocial Sciences (R0)