Abstract
While the cerebellum's role in motor function is well recognized, the nature of its concurrent role in cognitive function remains considerably less clear. The current consensus paper gathers diverse views on a variety of important roles played by the cerebellum across a range of cognitive and emotional functions. This paper considers the cerebellum in relation to neurocognitive development, language function, working memory, executive function, and the development of cerebellar internal control models and reflects upon some of the ways in which better understanding the cerebellum's status as a “supervised learning machine” can enrich our ability to understand human function and adaptation. As all contributors agree that the cerebellum plays a role in cognition, there is also an agreement that this conclusion remains highly inferential. Many conclusions about the role of the cerebellum in cognition originate from applying known information about cerebellar contributions to the coordination and quality of movement. These inferences are based on the uniformity of the cerebellum's compositional infrastructure and its apparent modular organization. There is considerable support for this view, based upon observations of patients with pathology within the cerebellum.
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Notes
Marvel note: funding source for this study: K01 DA030442 (NIH)
It is proposed that this feature of the nearly limitless blending of internal models of sound patterns with visual-spatial imagery explains the origin of what Hockett (185) referred to as the “duality of patterning” feature of language (meaningless sounds or symbols can be rearranged to produce an unlimited number of messages, e.g., Hockett described how Morse Code exemplifies this feature). Hockett argued that duality of patterning is unique to human language. However, since monkeys have shown fronto-cerebellar action in switching tools [170] indicating an open-ended synthesis of multiple visual-spatial internal models, duality of patterning appears to be shared, at least in nascent form, with other primate species, and, therefore, that duality patterning originates not in the tags that place moments of visual-spatial working memory in long-term memory, but in the limitless potential of internal models of those visual spatial moments themselves.
References
Schmahmann JD. The cerebellum and cognition. London: Academic; 1997.
Diamond A. Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Dev. 2000;71(1):44–56.
Baillieux H, Smet HJ, Paquier PF, De Deyn PP, Marien P. Cerebellar neurocognition: Insights into the bottom of the brain. Clin Neurol Neurosurg. 2008;110(8):763–73.
Kuper M, Dimitrova A, Thurling M, Maderwald S, Roths J, Elles HG, et al. Evidence for a motor and a non-motor domain in the human dentate nucleus—An fMRI study. Neuroimage. 2011;54(4):2612–22.
Molinari M, Chiricozzi FR, Clausi S, Tedesco AM, De LM, Leggio MG. Cerebellum and detection of sequences, from perception to cognition. Cerebellum. 2008;7(4):611–5.
Ito M. Movement and thought: identical control mechanisms by the cerebellum. Trends Neurosci. 1993;16(11):448–50.
Parvizi J. Corticocentric myopia: old bias in new cognitive sciences. Trends Cogn Sci. 2009;13(8):354–9.
Manto M, Haines D. Cerebellar research: two centuries of discoveries. The Cerebellum. 2012;11:446–8.
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45.
Sokolov AA, Erb M, Grodd W, Pavlova MA. Structural loop between the cerebellum and the superior temporal sulcus: evidence from diffusion tensor imaging. Cerebral Cortex. 2013;(in press).
Leiner HC, Leiner AL, Dow RS. Cognitive and language functions of the human cerebellum. Trends Neurosci. 1993;16(11):444–7.
Middleton FA, Strick PL. Basal ganglia and cerebellar output influences non-motor function. Mol Psychiatry. 1996;1(6):429–33.
Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65.
Balsters JH, Ramnani N. Symbolic representations of action in the human cerebellum. Neuroimage. 2008;43(2):388–98.
Shiffrin RM, Schneider W. Automatic and controlled processing revisited. Psychol Rev. 1984;91(2):269–76.
Blomfield S, Marr D. How the cerebellum may be used. Nature. 1970;227(5264):1224–8.
Marr D. A theory of cerebellar cortex. J Physiol. 1969;202(2):437–70.
Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.
Greger B, Norris S. Simple spike firing in the posterior lateral cerebellar cortex of Macaque Mulatta was correlated with success-failure during a visually guided reaching task. Exp Brain Res. 2005;167(4):660–5.
Gilbert PF, Thach WT. Purkinje cell activity during motor learning. Brain Res. 1977;128(2):309–28.
Ojakangas CL, Ebner TJ. Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J Neurophysiol. 1992;68(6):2222–36.
Medina JF, Lisberger SG. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci. 2008;11(10):1185–92.
Schmahmann JD, Rosene DL, Pandya DN. Motor projections to the basis pontis in rhesus monkey. J Comp Neurol. 2004;478(3):248–68.
Glickstein M, May III JG, Mercier BE. Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol. 1985;235(3):343–59.
Brodal P. The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain. 1978;101(2):251–83.
Prevosto V, Graf W, Ugolini G. Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex. 2010;20(1):214–28.
Ramnani N, Behrens TE, Johansen-Berg H, Richter MC, Pinsk MA, Andersson JL, et al. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cereb Cortex. 2006;16(6):811–8.
Ramnani N. Frontal lobe and posterior parietal contributions to the cortico-cerebellar system. Cerebellum. 2012;11(2):366–83.
Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.
Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23(23):8432–44.
Schmahmann JD, Pandya DN. Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol. 1989;289(1):53–73.
Schmahmann JD, Pandya DN. Prelunate, occipitotemporal, and parahippocampal projections to the basis pontis in rhesus monkey. J Comp Neurol. 1993;337(1):94–112.
Schmahmann JD, Pandya DN. Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neurosci Lett. 1995;199(3):175–8.
Schmahmann JD, Pandya DN. The cerebrocerebellar system. Int Rev Neurobiol. 1997;41:31–60.
Schmahmann JD, Pandya DN. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci. 1997;17(1):438–58.
Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7(7):511–22.
Balsters JH, Cussans E, Diedrichsen J, Phillips KA, Preuss TM, Rilling JK, et al. Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage. 2010;49(3):2045–52.
Bunge SA. How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci. 2004;4(4):564–79.
Platt ML, Glimcher PW. Neural correlates of decision variables in parietal cortex. Nature. 1999;400(6741):233–8.
Wallis JD, Anderson KC, Miller EK. Single neurons in prefrontal cortex encode abstract rules. Nature. 2001;411(6840):953–6.
Wallis JD, Miller EK. From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol. 2003;90(3):1790–806.
Miller EK, Nieder A, Freedman DJ, Wallis JD. Neural correlates of categories and concepts. Curr Opin Neurobiol. 2003;13(2):198–203.
O'Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2010;20(4):953–65.
Balsters JH, Ramnani N. Cerebellar plasticity and the automation of first-order rules. Journal of Neuroscience. 2011;31(6):2305–12.
Schmahmann JD. An emerging concept. The cerebellar contribution to higher function. Arch Neurol. 1991;48(11):1178–87.
Voogd J. Cerebellum and precerebellar nuclei. In: Paxinos G, Mai JK, editors. The human nervous system. 2nd ed. San Diego: Academic; 2004. p. 321–92.
Ito M. The cerebellum and neural control. New York: Raven Press; 1984.
Schmahmann JD. The role of the cerebellum in affect and psychosis. J Neurolinguistics. 2000;13(23):189–214.
Schmahmann JD. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn Sci. 1998;2(9):362–71.
Schmahmann JD. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev. 2010;20(3):236–60.
Schmahmann JD, Pandya DN. The cereberocerebellar system. In: Schmahmann JD, editor. The cerebellum and cognition. San Diego: Academic; 1997. p. 31–60.
Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.
Krienen FM, Buckner RL. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex. 2009;19(10):2485–97.
Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29(26):8586–94.
Grimaldi G, Manto M. Topography of cerebellar deficits in humans. Cerebellum. 2012;11(2):336–51.
Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.
Schmahmann JD, MacMore J, Vangel M. Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience. 2009;162(3):852–61.
Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain. 2011;134(Pt 12):3672–86.
Snider RC, Stowell A. Receiving areas of the tactile, auditory, and visual systems in the cerebellum. J Neurophysiol. 1944;7:331–57.
Schoch B, Dimitrova A, Gizewski ER, Timmann D. Functional localization in the human cerebellum based on voxelwise statistical analysis: a study of 90 patients. Neuroimage. 2006;30(1):36–51.
Levisohn L, Cronin-Golomb A, Schmahmann JD. Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain. 2000;123(Pt 5):1041–50.
Schmahmann JD. From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp. 1996;4(3):174–98.
Chheda M, Sherman J, Schmahmann JD. Neurologic, psychiatric and cognitive manifestations in cerebellar agenesis. Neurology. 2002;58 suppl 3:356.
Tavano A, Grasso R, Gagliardi C, Triulzi F, Bresolin N, Fabbro F, et al. Disorders of cognitive and affective development in cerebellar malformations. Brain. 2007;130(Pt 10):2646–60.
Geschwind DH. Focusing attention on cognitive impairment in spinocerebellar ataxia. Arch Neurol. 1999;56(1):20–2.
Thompson RF, Bao S, Chen L, Cipriano BD, Grethe JS, Kim JJ. Associative learning. In: Schmahmann JD, editor. The cerebellum and cognition. San Diego: Academic; 1997. p. 151–89.
Parvizi J, Joseph J, Press DZ, Schmahmann JD. Pathological laughter and crying in patients with multiple system atrophy-cerebellar type. Mov Disord. 2007;22(6):798–803.
Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67.
Demirtas-Tatlidede A, Freitas C, Cromer JR, Safar L, Ongur D, Stone WS, et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res. 2010;124(1–3):91–100.
Ito M. The modifiable neuronal network of the cerebellum. Jpn J Physiol. 1984;34(5):781.
Allen G, Courchesne E. The cerebellum and non-motor function: clinical implications. Mol Psychiatry. 1998;3(3):207–10.
Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 2004;16(3):367–78.
Lidzba K, Wilke M, Staudt M, Krageloh-Mann I, Grodd W. Reorganization of the cerebro-cerebellar network of language production in patients with congenital left-hemispheric brain lesions. Brain Lang. 2008;106(3):204–10.
Riva D. Higher cognitive function processing in developmental age: specialized areas, connections, and districuted networks. In: Riva D, Njiokiktjien C, Bulgheroni S, editors. Brain lesion localization and developmental functions. Montrouge, France: John Libbey Eurotext; 2011. p. 1–8.
Schmahmann JD, Pandya DN. Fiber pathways of the brain. USA: OUP; 2009.
Jissendi P, Baudry S, Baleriaux D. Diffusion tensor imaging (DTI) and tractography of the cerebellar projections to prefrontal and posterior parietal cortices: a study at 3T. J Neuroradiol. 2008;35(1):42–50.
Uddin LQ, Supekar K, Menon V. Typical and atypical development of functional human brain networks: insights from resting-state FMRI. Front Syst Neurosci. 2010;4:21.
Limperopoulos C, du Plessis AJ. Disorders of cerebellar growth and development. Curr Opin Pediatr. 2006;18(6):621–7.
Riva D, Giorgi C. The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain. 2000;123(Pt 5):1051–61.
Riva D, Vago C, Usilla A, Treccani C, Pantaleoni C, D'Arrigo S. The role of the cerebellum in processing higher cognitive and social functions in congenital and acquired disease in developmental age. In: Riva D, Njiokiktjien C, editors. Brain lesion localization and developmental functions. Montrouge, France: John Libbey Eurotext; 2010. p. 133–43.
Bolduc ME, Limperopoulos C. Neurodevelopmental outcomes in children with cerebellar malformations: a systematic review. Dev Med Child Neurol. 2009;51(4):256–67.
Riva D, Pantaleoni C, Nicheli F, Bulgheroni S, Bagnasco I. Cervelletto e funzioni psyichiche superiori in eta evolutiva: risultati preliminari in una serie di bambini con ipoplasia cerebellare congenita. Giorn Neuropsich Eta Evol. 2001;21:252–6.
Amaral DG, Schumann CM, Nordahl CW. Neuroanatomy of autism. Trends Neurosci. 2008;31(3):137–45.
Riva D, Annunziata S, Contarino V, Erbetta A, Aquino D, Bulgheroni S. Gray matter reduction in the vermis and CRUS-II is associated with social and interaction deficits in low-functioning children with autistic spectrum disorders: a VBM-DARTEL Study. Cerebellum 2013;(in press).
Riva D, Giorgi C. The contribution of the cerebellum to mental and social functions in developmental age. Fiziol Cheloveka. 2000;26(1):27–31.
Steinlin M, Imfeld S, Zulauf P, Boltshauser E, Lovblad KO, Ridolfi LA, et al. Neuropsychological long-term sequelae after posterior fossa tumour resection during childhood. Brain. 2003;126(Pt 9):1998–2008.
Scott RB, Stoodley CJ, Anslow P, Paul C, Stein JF, Sugden EM, et al. Lateralized cognitive deficits in children following cerebellar lesions. Dev Med Child Neurol. 2001;43(10):685–91.
Paquier P, van Mourik M, van Dongen H, Catsman-Berrevoets C, Brison A. Cerebellar mutism syndromes with subsequent dysarthria: a study of three children and a review of the literature. Rev Neurol (Paris). 2003;159(11):1017–27.
Riva D. The cerebellar contribution to language and sequential functions: evidence from a child with cerebellitis. Cortex. 1998;34(2):279–87.
Tavano A, Fabbro F, Borgatti R. Speaking without the cerebellum. In: Schalley AC, Khlentzos D, editors. Mental states. 1st ed. Amsterdam: John Benjamins Publishing Company; 2007. p. 171–90.
Bolduc ME, du Plessis AJ, Sullivan N, Khwaja OS, Zhang X, Barnes K, et al. Spectrum of neurodevelopmental disabilities in children with cerebellar malformations. Dev Med Child Neurol. 2011;53(5):409–16.
Ronning C, Sundet K, Due-Tonnessen B, Lundar T, Helseth E. Persistent cognitive dysfunction secondary to cerebellar injury in patients treated for posterior fossa tumors in childhood. Pediatr Neurosurg. 2005;41(1):15–21.
Manto MU. The wide spectrum of spinocerebellar ataxias (SCAs). Cerebellum. 2005;4(1):2–6.
Burk K. Cognition in hereditary ataxia. Cerebellum. 2007;6(3):280–6.
Lasek K, Lencer R, Gaser C, Hagenah J, Walter U, Wolters A, et al. Morphological basis for the spectrum of clinical deficits in spinocerebellar ataxia 17 (SCA17). Brain. 2006;129(Pt 9):2341–52.
Koziol LF, Budding DE. Subcortical structures and cognition: implications for neuropsychological assessment. New York: Springer; 2009.
Manto M, Lorivel T. Cognitive repercussions of hereditary cerebellar disorders. Cortex. 2011;47(1):81–100.
Lalonde R, Filali M, Bensoula AN, Lestienne F. Sensorimotor learning in three cerebellar mutant mice. Neurobiol Learn Mem. 1996;65(2):113–20.
Lalonde R, Strazielle C. Motor performance and regional brain metabolism of spontaneous murine mutations with cerebellar atrophy. Behav Brain Res. 2001;125(1):103–8.
D'Agata F, Caroppo P, Baudino B, Caglio M, Croce M, Bergui M, et al. The recognition of facial emotions in spinocerebellar ataxia patients. Cerebellum. 2011;10(3):600–10.
Kameya T, Abe K, Aoki M, Sahara M, Tobita M, Konno H, et al. Analysis of spinocerebellar ataxia type 1 (SCA1)-related CAG trinucleotide expansion in Japan. Neurology. 1995;45(8):1587–94.
Spadaro M, Giunti P, Lulli P, Frontali M, Jodice C, Cappellacci S, et al. HLA-linked spinocerebellar ataxia: a clinical and genetic study of large Italian kindreds. Acta Neurol Scand. 1992;85(4):257–65.
Giunti P, Sweeney MG, Spadaro M, Jodice C, Novelletto A, Malaspina P, et al. The trinucleotide repeat expansion on chromosome 6p (SCA1) in autosomal dominant cerebellar ataxias. Brain. 1994;117(Pt 4):645–9.
Sasaki H, Fukazawa T, Yanagihara T, Hamada T, Shima K, Matsumoto A, et al. Clinical features and natural history of spinocerebellar ataxia type 1. Acta Neurol Scand. 1996;93(1):64–71.
Storey E, Forrest SM, Shaw JH, Mitchell P, Gardner RJ. Spinocerebellar ataxia type 2: clinical features of a pedigree displaying prominent frontal-executive dysfunction. Arch Neurol. 1999;56(1):43–50.
Wadia NH. A variety of olivopontocerebellar atrophy distinguished by slow eye movements and peripheral neuropathy. Adv Neurol. 1984;41:149–77.
Burk K, Stevanin G, Didierjean O, Cancel G, Trottier Y, Skalej M, et al. Clinical and genetic analysis of three German kindreds with autosomal dominant cerebellar ataxia type I linked to the SCA2 locus. J Neurol. 1997;244(4):256–61.
Le PF, Zappala G, Saponara R, Domina E, Restivo D, Reggio E, et al. Cognitive findings in spinocerebellar ataxia type 2: relationship to genetic and clinical variables. J Neurol Sci. 2002;201(1–2):53–7.
Maruff P, Tyler P, Burt T, Currie B, Burns C, Currie J. Cognitive deficits in Machado–Joseph disease. Ann Neurol. 1996;40(3):421–7.
Riess O, Rüb U, Pastore A, Bauer P, Schöls L. SCA3: neurological features, pathogenesis and animal models. Cerebellum. 2008;7(2):125–37.
Coutinho P, Andrade C. Autosomal dominant system degeneration in Portuguese families of the Azores Islands. A new genetic disorder involving cerebellar, pyramidal, extrapyramidal and spinal cord motor functions. Neurology. 1978;28(7):703–9.
Fowler HL. Machado–Joseph–Azorean disease. A ten-year study. Arch Neurol. 1984;41(9):921–5.
Sequeiros J, Coutinho P. Epidemiology and clinical aspects of Machado–Joseph disease. Adv Neurol. 1993;61:139–53.
Globas C, Bosch S, Zuhlke C, Daum I, Dichgans J, Burk K. The cerebellum and cognition. Intellectual function in spinocerebellar ataxia type 6 (SCA6). J Neurol. 2003;250(12):1482–7.
Stevanin G, Durr A, Benammar N, Brice A. Spinocerebellar ataxia with mental retardation (SCA13). Cerebellum. 2005;4(1):43–6.
Tsuji S, Onodera O, Goto J, Nishizawa M. Sporadic ataxias in Japan: population-based epidemiological study. Cerebellum. 2008;7(2):189–97.
Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.
Andreasen NC, Oleary DS, Arndt S, Cizadlo T, Hurtig R, Rezai K, et al. Short-term and long-term verbal memory—a positron emission tomography study. Proc Natl Acad Sci U S A. 1995;92(11):5111–5.
Andreasen NC, Oleary DS, Arndt S, Cizadlo T, Rezai K, Watkins GL, et al. PET studies of memory: novel and practiced free recall of complex narratives.1. Neuroimage. 1995;2(4):284–95.
Andreasen NC, Oleary DS, Cizadlo T, Arndt S, Rezai K, Watkins GL, et al. PET studies of memory: novel versus practiced free recall of word lists.2. Neuroimage. 1995;2(4):296–305.
Andreasen NC, Oleary DS, Cizadlo T, Arndt S, Rezai K, Watkins L, et al. Remembering the past—2 facets of episodic memory explored with positron emission tomography. Am J Psychiatry. 1995;152(11):1576–85.
Andreasen NC, O'Leary DS, Paradiso S, Cizadlo T, Arndt S, Watkins GL, et al. The cerebellum plays a role in conscious episodic memory retrieval. Hum Brain Mapp. 1999;8(4):226–34.
Andreasen NC, Calarge CA, O'Leary DS. Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophr Bull. 2008;34(4):708–19.
Andreasen NC, Paradiso S, O'Leary DS. “Cognitive dysmetria” as an integrative theory of schizophrenia: a dysfunction in cortical subcortical-cerebellar circuitry? Schizophr Bull. 1998;24(2):203–18.
Wassink TH, Andreasen NC, Nopoulos P, Flaum M. Cerebellar morphology as a predictor of symptom and psychosocial outcome in schizophrenia. Biol Psychiatry. 1999;45(1):41–8.
Nopoulos PC, Ceilley JW, Gailis EA, Andreasen NC. An MRI study of cerebellar vermis morphology in patients with schizophrenia: Evidence in support of the cognitive dysmetria concept. Biol Psychiatry. 1999;46(5):703–11.
Andreasen NC, Cohen G, Harris G, Cizadlo T, Parkkinen J, Rezai K, et al. Image-processing for the study of brain structure and function—problems and programs. J Neuropsychiatry Clin Neurosci. 1992;4(2):125–33.
Andreasen NC, Oleary DS, Flaum M, Nopoulos P, Watkins GL, Ponto LLB, et al. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naive patients. Lancet. 1997;349(9067):1730–4.
Andreasen NC. Linking mind and brain in the study of mental illnesses: a project for a scientific psychopathology. Science. 1997;275(5306):1586–93.
Nopoulos P, Torres I, Flaum M, Andreasen NC, Ehrhardt JC, Yuh WTC. Brain morphology in first-episode schizophrenia. Am J Psychiatry. 1995;152(12):1721–3.
Nopoulos PC, Flaum M, Andreasen NC, Swayze VW. Gray-matter heterotopias in schizophrenia. Psychiatry Res-Neuroimaging. 1995;61(1):11–4.
Wiser AK, Andreasen NC, O'Leary DS, Watkins GL, Ponto LLB, Hichwa RD. Dysfunctional cortico-cerebellar circuits cause ‘cognitive dysmetria’ in schizophrenia. Neuroreport. 1998;9(8):1895–9.
Crespo-Facorro B, Kim JJ, Andreasen NC, O'Leary DS, Wiser AK, Bailey JM, et al. Human frontal cortex: an MRI-based parcellation method. Neuroimage. 1999;10(5):500–19.
Crespo-Facorro B, Wiser AK, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, et al. Neural basis of novel and well-learned recognition memory in schizophrenia: a positron emission tomography study. Hum Brain Mapp. 2001;12(4):219–31.
Crespo-Facorro B, Paradiso S, Andreasen NC, O'Leary DS, Watkins GL, Ponto LL, et al. Neural mechanisms of anhedonia in schizophrenia: a PET study of response to unpleasant and pleasant odors. JAMA. 2001;286(4):427–35.
Miller DD, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, Hichwa RD. Comparison of the effects of risperidone and haloperidol on regional cerebral blood flow in schizophrenia. Biol Psychiatry. 2001;49(8):704–15.
Magnotta VA, Adix ML, Caprahan A, Lim K, Gollub R, Andreasen NC. Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: a pilot study. Psychiatry Res. 2008;163(3):193–200.
Baddeley A. Working memory. Science. 1992;255(5044):556–9.
Baddeley A, Gathercole S, Papagno C. The phonological loop as a language learning device. Psychol Rev. 1998;105(1):158–73.
Aboitiz F, Garcia RR, Bosman C, Brunetti E. Cortical memory mechanisms and language origins. Brain Lang. 2006;98(1):40–56.
Gathercole SE, Baddeley AD. Evaluation of the role of phonological STM in the development of vocabulary in children: a longitudinal study. J Mem Lang. 1989;28(2):200–13.
Gathercole SE, Baddeley AD. Phonological memory deficits in language disordered children: is there a causal connection? J Mem Lang. 1990;29(3):336–60.
Wager TD, Smith EE. Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci. 2003;3(4):255–74.
Durisko C, Fiez JA. Functional activation in the cerebellum during working memory and simple speech tasks. Cortex. 2010;46(7):896–906.
Chen SH, Desmond JE. Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task. Neuropsychologia. 2005;43(9):1227–37.
Chang C, Crottaz-Herbette S, Menon V. Temporal dynamics of basal ganglia response and connectivity during verbal working memory. Neuroimage. 2007;34(3):1253–69.
Chein JM, Fiez JA. Dissociation of verbal working memory system components using a delayed serial recall task. Cereb Cortex. 2001;11(11):1003–14.
Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci. 1997;17(24):9675–85.
Marvel CL, Desmond JE. From storage to manipulation: how the neural correlates of verbal working memory reflect varying demands on inner speech. Brain Lang. 2012;120(1):42–51.
Hulsmann E, Erb M, Grodd W. From will to action: sequential cerebellar contributions to voluntary movement. Neuroimage. 2003;20(3):1485–92.
Marvel CL, Desmond JE. Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev. 2010;20(3):271–9.
Chen SH, Desmond JE. Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks. Neuroimage. 2005;24(2):332–8.
Ravizza SM, McCormick CA, Schlerf JE, Justus T, Ivry RB, Fiez JA. Cerebellar damage produces selective deficits in verbal working memory. Brain. 2006;129(Pt 2):306–20.
Ackermann H, Mathiak K, Riecker A. The contribution of the cerebellum to speech production and speech perception: clinical and functional imaging data. Cerebellum. 2007;6(3):202–13.
Ackermann H, Mathiak K, Ivry RB. Temporal organization of “internal speech” as a basis for cerebellar modulation of cognitive functions. Behav Cogn Neurosci Rev. 2004;3(1):14–22.
Desmond JE, Chen SH, DeRosa E, Pryor MR, Pfefferbaum A, Sullivan EV. Increased frontocerebellar activation in alcoholics during verbal working memory: an fMRI study. Neuroimage. 2003;19(4):1510–20.
Marvel CL, Faulkner ML, Strain EC, Mintzer MZ, Desmond JE. An fMRI investigation of cerebellar function during verbal working memory in methadone maintenance patients. Cerebellum. 2012;11(1):300–10.
Silverman DH, Dy CJ, Castellon SA, Lai J, Pio BS, Abraham L, et al. Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5–10 years after chemotherapy. Breast Cancer Res Treat. 2007;103(3):303–11.
Sweet LH, Rao SM, Primeau M, Mayer AR, Cohen RA. Functional magnetic resonance imaging of working memory among multiple sclerosis patients. J Neuroimaging. 2004;14(2):150–7.
Valera EM, Faraone SV, Biederman J, Poldrack RA, Seidman LJ. Functional neuroanatomy of working memory in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry. 2005;57(5):439–47.
Beneventi H, Tonnessen FE, Ersland L, Hugdahl K. Working memory deficit in dyslexia: behavioral and FMRI evidence. Int J Neurosci. 2010;120(1):51–9.
Koch K, Wagner G, Schachtzabel C, Schultz C, Sauer H, Schlosser RG. Association between learning capabilities and practice-related activation changes in schizophrenia. Schizophr Bull. 2010;36(3):486–95.
White T, Schmidt M, Kim DI, Calhoun VD. Disrupted functional brain connectivity during verbal working memory in children and adolescents with schizophrenia. Cereb Cortex. 2011;21(3):510–8.
Leiner HC, Leiner AL, Dow RS. Does the cerebellum contribute to mental skills? Behav Neurosci. 1986;100(4):443–54.
Leiner HC, Leiner AL, Dow RS. Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? Behav Neurosci. 1989;103(5):998–1008.
Imamizu H, Higuchi S, Toda A, Kawato M. Reorganization of brain activity for multiple internal models after short but intensive training. Cortex. 2007;43(3):338–49.
Goldman-Rakic PS. Working memory and the mind. Sci Am. 1992;267(3):110–7.
Miyake A. Models of working memory: mechanisms of active maintenance and executive control. Cambridge: Cambridge University Press; 1999.
Fragaszy DM, Cummins-Sebree SE. Relational spatial reasoning by a nonhuman: the example of capuchin monkeys. Behav Cogn Neurosci Rev. 2005;4(4):282–306.
Obayashi S, Matsumoto R, Suhara T, Nagai Y, Iriki A, Maeda J. Functional organization of monkey brain for abstract operation. Cortex. 2007;43(3):389–96.
Vandervert L. The evolution of language: the cerebro-cerebellar blending of visual–spatial working memory with vocalizations. J Mind Behav. 2011;32(4):317.
Vandervert LR. The evolution of Mandler's conceptual primitives (image-schemas) as neural mechanisms for space–time simulation structures. New Ideas Psychol. 1997;15(2):105–23.
Vandervert L. How working memory and cognitive modeling functions of the cerebellum contribute to discoveries in mathematics. New Ideas Psychol. 2003;21(2):159–75.
Vandervert LR. The appearance of the child prodigy 10,000 years ago: an evolutionary and developmental explanation. J Mind Behav. 2009;30(1):15.
Vandervert LR, Schimpf PH, Liu H. How working memory and the cerebellum collaborate to produce creativity and innovation. Creat Res J. 2007;19(1):1–18.
Imamizu H, Kawato M. Brain mechanisms for predictive control by switching internal models: implications for higher-order cognitive functions. Psychol Res. 2009;73(4):527–44.
Flanagan JR, Nakano E, Imamizu H, Osu R, Yoshioka T, Kawato M. Composition and decomposition of internal models in motor learning under altered kinematic and dynamic environments. J Neurosci. 1999;19(20):RC34.
Nakano E. Composition and decomposition learning of reaching movements under altered environments: an examination of the multiplicity of internal models. Syst Comput Japan. 2002;33(11):80.
Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M. Modular organization of internal models of tools in the human cerebellum. Proc Natl Acad Sci U S A. 2003;100(9):5461–6.
Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000;403(6766):192–5.
Chomsky N. Cartesian linguistics: a chapter in the history of rationalist thought. New York: Harper & Row; 1966.
Baddeley AD, Andrade J. Working memory and the vividness of imagery. J Exp Psychol Gen. 2000;129(1):126–45.
Tooby J, DeVore I. The reconstruction of hominid behavioral evolution through strategic modeling. In: Kinzey WG, editor. The evolution of human behavior: primate models. Albany, NY: State University of New York Press; 1987. p. 183–237.
Pinker S. Colloquium paper: the cognitive niche: coevolution of intelligence, sociality, and language. Proc Natl Acad Sci U S A. 2010;107 Suppl 2:8993–9.
Hockett CF. The origin of speech. San Francisco, CA: W.H. Freeman and Co; 1960.
Cisek P, Kalaska JF. Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci. 2010;33:269–98.
Doya K. What are the computations of the cerebellum, the basal ganglia and the cerebral cortex? Neural Netw. 1999;12(7–8):961–74.
Houk JC, Wise SP. Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. Cereb Cortex. 1995;5(2):95–110.
Pezzulo G, Barsalou LW, Cangelosi A, Fischer MH, McRae K, Spivey M. Computational grounded cognition: a new alliance between grounded cognition and computational modeling. Frontiers in Psychology 2013;(in press).
Desmurget M, Grafton S. Forward modeling allows feedback control for fast reaching movements. Trends Cogn Sci. 2000;4(11):423–31.
Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.
D'Angelo E. The cerebellar network: revisiting the critical issues. J Physiol. 2011;589(Pt 14):3421–2.
Frens MA, Donchin O. Forward models and state estimation in compensatory eye movements. Front Cell Neurosci. 2009;3:13.
Kawato M. Internal models for motor control and trajectory planning. Curr Opin Neurobiol. 1999;9(6):718–27.
Wolpert DM, Miall RC. Forward models for physiological motor control. Neural Netw. 1996;9(8):1265–79.
Shadmehr R, Krakauer JW. A computational neuroanatomy for motor control. Exp Brain Res. 2008;185(3):359–81.
Pezzulo G. Grounding procedural and declarative knowledge in sensorimotor anticipation. Mind Lang. 2011;26(1):78–114.
Pezzulo G, Castelfranchi C. Thinking as the control of imagination: a conceptual framework for goal-directed systems. Psychol Res. 2009;73(4):559–77.
Pezzulo G, Castelfranchi C. The symbol detachment problem. Cogn Process. 2007;8(2):115–31.
Hesslow G. Conscious thought as simulation of behaviour and perception. Trends Cogn Sci. 2002;6(6):242–7.
Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage. 2001;14(1):S103–9.
Grush R. The emulation theory of representation: motor control, imagery, and perception. Behav Brain Sci. 2004;27(3):377–96.
Friston K. The free-energy principle: a unified brain theory? Nat Rev Neurosci. 2010;11(2):127–38.
Schubotz RI. Prediction of external events with our motor system: towards a new framework. Trends Cogn Sci. 2007;11(5):211–8.
Imamizu H, Kawato M. Cerebellar internal models: implications for the dexterous use of tools. Cerebellum. 2010;22:1–11.
Wolpert DM, Doya K, Kawato M. A unifying computational framework for motor control and social interaction. Philos Trans R Soc Lond B Biol Sci. 2003;358(1431):593–602.
Pezzulo G, Dindo H. What should I do next? Using shared representations to solve interaction problems. Exp Brain Res. 2011;211(3–4):613–30.
Middleton FA, Strick PL. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994;266(5184):458–61.
Pezzulo G. An active inference view of cognitive control. Front Psychol. 2012;3:478.
Barsalou LW. Grounded cognition. Annu Rev Psychol. 2008;59:617–45.
Pezzulo G, Barsalou LW, Cangelosi A, Fischer MH, McRae K, Spivey MJ. The mechanics of embodiment: a dialog on embodiment and computational modeling. Front Psychol. 2011;2:5.
Pezzulo G, Barsalou LW, Cangelosi A, Fischer MH, McRae K, Spivey MJ. Computational grounded cognition: a new alliance between grounded cognition and computational modeling. Front Psychol. 2012;3:612.
Moulton ST, Kosslyn SM. Imagining predictions: mental imagery as mental emulation. Philos Trans R Soc Lond B Biol Sci. 2009;364(1521):1273–80.
Barkley RA. The executive functions and self-regulation: an evolutionary neuropsychological perspective. Neuropsychol Rev. 2001;11(1):1–29.
Glenberg AM. What memory is for. Behav Brain Sci. 1997;20(1):1–19.
Rosenbaum DA, Carlson RA, Gilmore RO. Acquisition of intellectual and perceptual-motor skills. Annu Rev Psychol. 2001;52:453–70.
Piaget J. The construction of reality in the child. New York: Basic Books; 1954.
Pezzulo G, Barca L, Bocconi AL, Borghi AM. When affordances climb into your mind: advantages of motor simulation in a memory task performed by novice and expert rock climbers. Brain Cogn. 2010;73(1):68–73.
Kawato M, Furukawa K, Suzuki R. A hierarchical neural-network model for control and learning of voluntary movement. Biol Cybern. 1987;57(3):169–85.
Wolpert DM, Ghahramani Z, Jordan MI. An internal model for sensorimotor integration. In: Science-New York Then Washington. Washington, DC: American Association for the Advancement of Science;1995. p. 1880
Flanagan JR, Wing AM. The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci. 1997;17(4):1519–28.
Mehta B, Schaal S. Forward models in visuomotor control. J Neurophysiol. 2002;88(2):942–53.
Higuchi S, Imamizu H, Kawato M. Cerebellar activity evoked by common tool-use execution and imagery tasks: an fMRI study. Cortex. 2007;43(3):350–8.
Imamizu H, Kuroda T, Yoshioka T, Kawato M. Functional magnetic resonance imaging examination of two modular architectures for switching multiple internal models. J Neurosci. 2004;24(5):1173–81.
Imamizu H, Kawato M. Neural correlates of predictive and postdictive switching mechanisms for internal models. J Neurosci. 2008;28(42):10751.
Iriki A. The neural origins and implications of imitation, mirror neurons and tool use. Curr Opin Neurobiol. 2006;16(6):660–7.
Johnson-Frey SH. The neural bases of complex tool use in humans. Trends Cogn Sci. 2004;8(2):71–8.
Glickstein M, Sultan F, Voogd J. Functional localization in the cerebellum. Cortex. 2011;47(1):59–80.
Rosenblatt F. Principles of neurodynamics. Washington: Spartan Books; 1962.
Fujita M. Adaptive filter model of the cerebellum. Biol Cybern. 1982;45(3):195–206.
Dean P, Porrill J, Ekerot CF, Jorntell H. The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci. 2010;11(1):30–43.
Barlow JS. The cerebellum and adaptive control. Cambridge, UK: Cambridge University Press; 2002.
Zaknich A. Principles of adaptive filters and self-learning systems. 2005. http://site.ebrary.com/id/10228674
Hebb DO. The organization of behavior; a neuropsychological theory. New York: Wiley; 1949.
Ito M. Bases and implications of learning in the cerebellum—adaptive control and internal model mechanism. Prog Brain Res. 2005;148:95–109.
Craik KJW. The nature of explanation. Cambridge: University Press; 1952.
Johnson-Laird PN. Mental models : towards a cognitive science of language, inference, and consciousness. Cambridge, Mass: Harvard University Press; 1983.
Piaget J. The psychology of intelligence. London: Routledge & Paul; 1950.
Ito M. The cerebellum: brain for an implicit self. Upper Saddle River, NJ: Ft Press; 2011.
McCarthy J, Minsky ML, Rochester N, Shannon CE. A proposal for the Dartmouth summer research project on artificial intelligence, August 31, 1955. AI Mag. 2006;27(4):12.
Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Brain. 1996;119(Pt 4):1199–211.
Koziol LF, Budding DE, Chidekel D. From movement to thought: executive function, embodied cognition, and the cerebellum. Cerebellum. 2012;11(2):505–25.
Penhune VB, Steele CJ. Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav Brain Res. 2012;226(2):579–91.
Jirenhed DA, Bengtsson F, Hesslow G. Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci. 2007;27(10):2493–502.
Hirata Y, Lockard JM, Highstein SM. Capacity of vertical VOR adaptation in squirrel monkey. J Neurophysiol. 2002;88(6):3194–207.
Kramer PD, Shelhamer M, Zee DS. Short-term adaptation of the phase of the vestibulo-ocular reflex (VOR) in normal human subjects. Exp Brain Res. 1995;106(2):318–26.
Gluck MA, Reifsnider ES, Thompson RF. Adaptive signal processing and the cerebellum: models of classical conditioning and VOR adaptation. In: Gluck MA, Rumelhart DE, editors. Neuroscience and connectionist theory. Hillsdale, NJ: Lawrence Erlbaum; 1990. p. 131–86.
Mauk MD, Donegan NH. A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn Mem. 1997;4(1):130–58.
Yamazaki T, Nagao S. A computational mechanism for unified gain and timing control in the cerebellum. PLoS One. 2012;7(3):e33319.
Smaers JB, Steele J, Zilles K. Modeling the evolution of cortico cerebellar systems in primates. Ann NY Acad Sci. 2011;1225(1):176–90.
Njiokiktjien C. Developmental dyspraxias: assessment and differential diagnosis. In: Riva D, Njiokiktjien C, editors. Brain lesion localization and developmental functions. Montrouge, France: John Libbey Eurotext; 2010. p. 157–86.
Galea JM, Vazquez A, Pasricha N, Orban de Xivry JJ, Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cerebral Cortex. 2011;21:1761–70.
Kalashnikova LA, Zueva YV, Pugacheva OV, Korsakova NK. Cognitive impairments in cerebellar infarcts. Neurosci Behav Physiol. 2005;35(8):773–9.
Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64(2):81–8.
Allen G, Courchesne E. Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. Am J Psychiatry. 2003;160(2):262–73.
Hopyan T, Laughlin S, Dennis M. Emotions and their cognitive control in children with cerebellar tumors. J Int Neuropsychol Soc. 2010;16(6):1027–38.
Wadsworth HM, Kana RK. Brain mechanisms of perceiving tools and imagining tool use acts: a functional MRI study. Neuropsychologia. 2011;49:1863–9.
Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, et al. Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol. 2009;5(5):e1000381.
Poldrack RA, Mumford JA, Schonberg T, Kalar D, Barman B, Yarkoni T. Discovering relations between mind, brain, and mental disorders using topic mapping. PLoS Comput Biol. 2012;8(10):e1002707.
Dobromyslin VI, Salat DH, Fortier CB, Leritz EC, Beckmann CF, Milberg WP, et al. Distinct functional networks within the cerebellum and their relation to cortical systems assessed with independent component analysis. Neuroimage. 2012;60(4):2073–85.
Wang D, Buckner RL, Liu H. Cerebellar asymmetry and its relation to cerebral asymmetry estimated by intrinsic functional connectivity. J Neurophysiol. 2013;109(1):46–57.
Stoodley CJ, Valera EM, Schmahmann JD. An fMRI case study of functional topography in the human cerebellum. Behav Neurol. 2010;23:65–79.
Schmahmann JD, Doyon J, Toga A, Petrides M, Evans A. MRI atlas of the human cerebellum. San Diego: Academic. 2000
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Koziol, L.F., Budding, D., Andreasen, N. et al. Consensus Paper: The Cerebellum's Role in Movement and Cognition. Cerebellum 13, 151–177 (2014). https://doi.org/10.1007/s12311-013-0511-x
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DOI: https://doi.org/10.1007/s12311-013-0511-x