Abstract
The cognitive neuroscience of the cerebellum is now an established multidisciplinary field of investigation. This essay traces the historical evolution of this line of inquiry from an emerging field to its current status, with personal reflections over almost three decades on this journey of discovery. It pays tribute to early investigators who recognized the wider role of the cerebellum beyond motor control, traces the origins of new terms and concepts including the dysmetria of thought theory, the universal cerebellar transform, and the cerebellar cognitive affective syndrome, and places these developments within the broader context of the scientific efforts of a growing community of cerebellar cognitive neuroscientists. This account considers the converging evidence from theoretical, anatomical, physiological, clinical, and functional neuroimaging approaches that have resulted in the transition from recognizing the cerebellar incorporation into the distributed neural circuits subserving cognition and emotion, to a hopeful new era of treatment of neurocognitive and neuropsychiatric manifestations of cerebellar diseases, and to cerebellar-based interventions for psychiatric disorders.
Similar content being viewed by others
References
Abbie, A. A. (1934). The projection of the forebrain on the pons and cerebellum. Proceedings of the Royal Society of London [Biol.] 115504–115522.
Albus, J. S. (1971). A theory of cerebellar function. Mathematical Biosciences, 10, 25–61.
Aleman, A., Sommer, I. E., & Kahn, R. S. (2007). Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. The Journal of Clinical Psychiatry, 68(3), 416–421.
Allen, G. I., & Tsukahara, N. (1974). Cerebrocerebellar communication systems. Physiological Reviews, 54(4), 957–1006.
Andreasen, N. C., O’Leary, D. S., Cizadlo, T., Arndt, S., Rezai, K., Ponto, L. L., et al. (1996). Schizophrenia and cognitive dysmetria: a positron emission tomography study of dysfunctional prefrontal-thalamic-cerebelar circuitry. Proceedings of the National Academy of Sciences of the United States of America, 93, 9985–9990.
Angevine, J. B., Mancall, E. L., & Yakovlev, P. I. (1961). The human cerebellum: An atlas of gross topography in serial sections. Boston: Little, Brown and Co.
Baillieux, H., De Smet, H. J., Dobbeleir, A., Paquier, P. F., De Deyn, P. P., & Mariën, P. (2010). Cognitive and affective disturbances following focal cerebellar damage in adults: a neuropsychological and SPECT study. Cortex, 46(7), 869–879.
Ball, G., Micco, D. J., & Berntson, G. (1974). Cerebellar stimulation in the rat. Complex stimulation bound oral behaviors and self-stimulation. Physiology & Behavior, 13, 123–127.
Barlow, J. S. (2002). The cerebellum and adaptive control. New York: Cambridge University Press.
Bauman, M., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35(6), 866–874.
Berman, A. F., Berman, D., & Prescott, J. W. (1978). The effect of cerebellar lesions on emotional behavior in the rhesus monkey. In I. S. Cooper, M. Riklan, & R. S. Snider (Eds.), The cerebellum, epilepsy and behavior (pp. 277–284). New York: Plenum. Adapted and reprinted as Berman, A. J. (1997). Amelioration of aggression: Response to selective cerebellar lesions in the rhesus monkey. In J. D. Schmahmann (Ed.), The cerebellum and cognition. Int Rev Neurobiol, 41, 111–119. San Diego: Academic.
Berntson, G. G., Potolicchio, S. J., Jr., & Miller, N. E. (1973). Evidence for higher functions of the cerebellum: eating and grooming elicited by cerebellar stimulation in cats. Proceedings of the National Academy of Sciences of the United States of America, 70(9), 2497–2499.
Bishop, D. V. (2007). Curing dyslexia and attention-deficit hyperactivity disorder by training motor co-ordination: miracle or myth? Journal of Paediatrics and Child Health, 43(10), 653–655.
Botez-Marquard, T., & Botez, M. I. (1993). Cognitive behavior in heredodegenerative ataxias. European Neurology, 33(5), 351–357.
Botez, M. I., Gravel, J., Attig, E., & Vezina, J. L. (1985). Reversible chronic cerebellar ataxia after phenytoin intoxication: possible role of cerebellum in cognitive thought. Neurology, 35(8), 1152–1157.
Bower, J. M. (1995). The cerebellum as sensory acquisition controller. Human Brain Mapping, 2, 12–13.
Brodal, P. (1978). The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain, 101(2), 251–283.
Brodal, A. (1981). Neurological anatomy in relation to clinical medicine (3rd ed.). New York: Oxford University Press.
Cannon, W. B. (1939). Law of denervation. American Journal of Medical Science 198(737–50).
Caplan, L. R., Schmahmann, J. D., Kase, C. S., Feldmann, E., Baquis, G., Greenberg, J. P., et al. (1990). Caudate Infarcts. Archives of Neurology, 47, 133–143.
Catani, M., Jones, D. K., Daly, E., Embiricos, N., Deeley, Q., Pugliese, L., et al. (2008). Altered cerebellar feedback projections in Asperger syndrome. Neuroimage, 41(4), 1184–1191.
Chambers, W. W., & Sprague, J. M. (1955a). Functional localization in the cerebellum. I. Organization in longitudinal cortico-nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. The Journal of Comparative Neurology, 103(1), 105–129.
Chambers, W. W., & Sprague, J. M. (1955b). Functional localization in the cerebellum. II. Somatotopic organization in cortex and nuclei. A.M.A. Archives of Neurology & Psychiatry, 74(6), 653–680.
Chheda, M., Sherman, J., & Schmahmann, J. D. (2002). Neurologic, psychiatric and cognitive manifestations in cerebellar agenesis. Neurology, 58(Suppl 3), 356.
Clarke, E., & O’Malley, C. D. (1996). The human brain and spinal cord. A historical study illustrated by writings from antiquity to the twentieth century (2nd ed.). San Francisco: Norman.
Clower, D. M., West, R. A., Lynch, J. C., & Strick, P. L. (2001). The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. The Journal of Neuroscience, 21(16), 6283–6291.
Combettes. (1831). Absence complète du cervelet, des pédoncules postérieurs et de la protubérance cérébrale chez une jeune fille morte dans sa onzième année. Bulletins de la Societe anatomique de Paris, 5, 148–157.
Cooper, I. S., Amin, L., & Gilman, S. W. J. M. (1974). The effect of chronic stimulation of cerebellar cortex on epilepsy in man. In I. S. Cooper, M. Riklan, & R. S. Snider (Eds.), The cerebellum, epilepsy and behavior (pp. 119–172). New York: Plenum.
Cooper, I. S., Riklan, M., Amin, I., & Cullinan, T. (1978). A long-term follow-up study of cerebellar stimulation for the control of epilepsy. In I. S. Cooper (Ed.), Cerebellar stimulation in man (pp. 19–38). New York: Raven.
Courchesne, E., & Allen, G. (1997). Prediction and preparation, fundamental functions of the cerebellum. Learning & Memory, 4(1), 1–35.
Courchesne, E., Yeung-Courchesne, R., Press, G. A., Hesselink, J. R., & Jernigan, T. L. (1988). Hypoplasia of cerebellar vermal lobules VI and VII in autism. The New England Journal of Medicine, 318(21), 1349–1354.
Cowan, W. M., Gottlieb, D. I., Hendrickson, A. E., Price, J. L., & Woolsey, T. A. (1972). The autoradiographic demonstration of axonal connections in the central nervous system. Brain Research, 37, 21–51.
Dejerine, J. J. (1895). Anatomie des centres nerveux. Paris: Rueff et Cie.
Demirtas-Tatlidede, A., Freitas, C., Cromer, J., Safar, L., Ongur, D., & Stone, W. S., et al. (2010). A proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophrenia Research, doi:10.1016/j.schres.2010.08.015
Denny-Brown, D. (1942). The sequelae of war head injuries. New England Journal of Medicine, 227, 771–789 and 813–821.
Denny-Brown, D. (1962). The Basal Ganglia and their relation to disorders of movement. London: Oxford University Press.
Denny-Brown, D. (1964). Department of neurology. In J. J. Byrne (Ed.), A history of the Boston City Hospital, 1905–1964 (pp. 110–122). Boston: Sheldon.
Denny-Brown, D., & Banker, B. Q. (1954). Amorphosynthesis from left parietal lesion. AMA Archives of Neurology and Psychiatry, 71, 302–313.
Denny-Brown, D., & Chambers, R. A. (1958). The parietal lobe and behavior. Research Publications - Association for Research in Nervous and Mental Disease, 36, 35–117.
Denny-Brown, D., Meyer, J. S., & Horenstein, S. (1952). The significance of perceptual rivalry resulting from parietal lesion. Brain, 75(4), 433–471.
Desmond, J. E., & Fiez, J. A. (1998). Neuroimaging studies of the cerebellum: language, learning and memory. Trends in Cognitive Sciences, 2, 355–362.
Diedrichsen, J. (2006). A spatially unbiased atlas template of the human cerebellum. Neuroimage, 33(1), 127–138.
Dietrichs, E., & Haines, D. E. (1984). Demonstration of hypothalamo-cerebellar and cerebello-hypothalamic fibres in a prosimian primate (Galago crassicaudatus). Anatomy and Embryology (Berlin), 170(3), 313–318.
Dimitrova, A., Zeljko, D., Schwarze, F., Maschke, M., Gerwig, M., Frings, M., et al. (2006). Probabilistic 3D MRI atlas of the human cerebellar dentate/interposed nuclei. Neuroimage, 30(1), 12–25.
Dow, R. S. (1974). Some novel concepts of cerebellar physiology. The Mount Sinai Journal of Medicine, 41(1), 103–119.
Dow, R. S., & Moruzzi, G. (1958). The physiology and pathology of the cerebellum. Minneapolis: University of Minnesota Press.
Doyon, J., Penhune, V., Ungerleider, L. G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41(3), 252–262.
Dum, R. P., & Strick, P. L. (2003). An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. Journal of Neurophysiology, 89(1), 634–639.
Duncan, G. W., Parker, S. W., & Fisher, C. M. (1975). Acute cerebellar infarction in the PICA territory. Archives of Neurology, 32(6), 364–368.
Evarts, E. V., & Thach, W. T. (1969). Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annual Review of Physiology, 31, 451–498.
Exner, C., Weniger, G., & Irle, E. (2004). Cerebellar lesions in the PICA but not SCA territory impair cognition. Neurology, 63(11), 2132–2135.
Fiez, J. A., & Raichle, M. E. (1997). Linguistic processing. In J. D. Schmahmann (Ed.), The cerebellum and cognition. Int Rev Neurobiol, 41, 233–254. San Diego: Academic.
Flourens, P. (1824). Recherches experimentales sur les proprietes et les fonctions du systseme nerveux, dans les animaux vertebres. Paris: Crevot.
Fox, P. T., Raichle, M. E., & Thach, W. T. (1985). Functional mapping of the human cerebellum with positron emission tomography. Proceedings of the National Academy of Sciences of the United States of America, 82(21), 7462–7466.
Fregni, F., Marcolin, M. A., Myczkowski, M., Amiaz, R., Hasey, G., Rumi, D. O., et al. (2006). Predictors of antidepressant response in clinical trials of transcranial magnetic stimulation. The International Journal of Neuropsychopharmacology, 9(6), 641–654.
Frick, R. B. (1982). The ego and the vestibulocerebellar system: some theoretical perspectives. The Psychoanalytic Quarterly, 51(1), 93–122.
Fries, W. (1990). Pontine projection from striate and prestriate visual cortex in the macaque monkey: an anterograde study. Visual Neuroscience, 4(3), 205–216.
Gall, F. J., Vimont, J., & Broussais, J. V. (1838). On the functions of the cerebellum. English translation by George Combe. Edinburgh: Maclachlan & Stewart.
Geschwind, N. (1965a). Disconnexion syndromes in animals and man. I. Brain, 88(2), 237–294.
Geschwind, N. (1965b). Disconnexion syndromes in animals and man. II. Brain, 88(3), 585–644.
Glickstein, M., May, J. G., 3rd, & Mercier, B. E. (1985). Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. The Journal of Comparative Neurology, 235(3), 343–359.
Gomez Beldarrain, M., Garcia-Monco, J. C., Quintana, J. M., Llorens, V., & Rodeno, E. (1997). Diaschisis and neuropsychological performance after cerebellar stroke. European Neurology, 37(2), 82–89.
Granziera, C., Schmahmann, J. D., Hadjikhani, N., Heiko, M., Meuli, R., Wedeen, V. J., et al. (2009). Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum in vivo. PLoS ONE, 4(4), e5101. Epub 2009 Apr 2.
Graybiel, A. M. (1998). The basal ganglia and chunking of action repertoires. Neurobiology of Learning and Memory, 70(1–2), 119–136.
Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C. F., Menon, V., et al. (2009). Distinct cerebellar contributions to intrinsic connectivity networks. The Journal of Neuroscience, 29(26), 8586–8594.
Haines, D. E., & Rubertone, J. A. (1977). Cerebellar corticonuclear fibers: evidence of zones in the primate anterior lobe. Neuroscience Letters, 6(2–3), 231–236.
Haines, D. E., & Dietrichs, E. (1984). An HRP study of hypothalamo-cerebellar and cerebello-hypothalamic connections in squirrel monkey (Saimiri sciureus). The Journal of Comparative Neurology, 229(4), 559–575.
Harlow, H. F., & Harlow, M. (1962). Social deprivation in monkeys. Scientific American, 207, 136–146.
Harper, J. W., & Heath, R. G. (1973). Anatomic connections of the fastigial nucleus to the rostral forebrain in the cat. Experimental Neurology, 39(2), 285–292.
Hartmann-von Monakow, K., Akert, K., & Kunzle, H. (1981). Projection of precentral, premotor and prefrontal cortex to the basilar pontine grey and to nucleus reticularis tegmenti pontis in the monkey (Macaca fascicularis). Schweizer Archiv für Neurologie, Neurochirurgie und Psychiatrie, 129(2), 189–208.
Heath, R. G. (1977). Modulation of emotion with a brain pacemaker. Treatment for intractable psychiatric illness. The Journal of Nervous and Mental Disease, 165(5), 300–317.
Heath, R. G. (1997). Foreword. In J. D. Schmahmann (Ed.), The Cerebellum and Cognition. Int Rev Neurobiol, 41, xxiii–xxv. San Diego: Academic.
Heath, R. G., & Harper, J. W. (1974). Ascending projections of the cerebellar fastigial nucleus to the hippocampus, amygdala, and other temporal lobe sites: evoked potential and histological studies in monkeys and cats. Experimental Neurology, 45(2), 268–287.
Heath, R. G., Franklin, D. E., & Shraberg, D. (1979). Gross pathology of the cerebellum in patients diagnosed and treated as functional psychiatric disorders. The Journal of Nervous and Mental Disease, 167(10), 585–592.
Heath, R. G., Llewellyn, R. C., & Rouchell, A. M. (1980). The cerebellar pacemaker for intractable behavioral disorders and epilepsy: follow-up report. Biological Psychiatry, 15(2), 243–256.
Heilman, K. M., Bowers, D., Valenstein, E., & Watson, R. T. (1986). The right hemisphere: neuropsychological functions. Journal of Neurosurgery, 64(5), 693–704.
Heilman, K. M., & Van Den Abell, T. (1980). Right hemisphere dominance for attention: the mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology, 30(3), 327–330.
Henneman, E., Cooke, P. M., & Snider, R. S. (1952). Cerebellar projections to the cerebral cortex. Research Publications—Association for Research in Nervous and Mental Disease, 30, 317–333.
Hornyak, M., Rovit, R. L., Simon, A. S., & Couldwell, W. T. (2001). Irving S. Cooper and the early surgical management of movement disorders. Video history. Neurosurgical Focus, 11(2), E6.
Ito, M. (1984). The cerebellum and neural control. New York: Raven.
Ito, M. (1993). Movement and thought: identical control mechanisms by the cerebellum. Trends in Neurosciences, 16(11), 448–450. discussion 453–444.
Ivry, R. B., & Keele, S. W. (1989). Timing functions of the cerebellum. Journal of Cognitive Neuroscience, 1, 136–152.
Jansen, J., & Brodal, A. (1940). Experimental studies on the intrinsic fibers of the cerebellum. II. The cortico-nuclear projection. The Journal of Comparative Neurology, 73, 267–321.
Joseph, A. B., Anderson, W. H., & O’Leary, D. H. (1985). Brainstem and vermis atrophy in catatonia. The American Journal of Psychiatry, 142(3), 352–354.
Kelly, R. M., & Strick, P. L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. The Journal of Neuroscience, 23(23), 8432–8444.
Kemper, T. L., & Bauman, M. (1998). Neuropathology of infantile autism. Journal of Neuropathology and Experimental Neurology, 57(7), 645–652.
Kim, J. J., Mohamed, S., Andreasen, N. C., O’Leary, D. S., Watkins, G. L., Boles Ponto, L. L., et al. (2000). Regional neural dysfunctions in chronic schizophrenia studied with positron emission tomography. The American Journal of Psychiatry, 157(4), 542–548.
Krienen, F. M., & Buckner, R. L. (2009). Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cerebral Cortex, 19(10), 2485–2497.
Kuypers, H. G., & Ugolini, G. (1990). Viruses as transneuronal tracers. Trends in Neurosciences, 13(2), 71–75.
Laird, A. R., Fox, P. M., Price, C. J., Glahn, D. C., Uecker, A. M., Lancaster, J. L., et al. (2005). ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Human Brain Mapping, 25(1), 155–164.
Lalonde, R., & Botez, M. I. (1986). Navigational deficits in weaver mutant mice. Brain Research, 398(1), 175–177.
Larsell, O., & Jansen, J. (1972). The comparative anatomy and histology of the cerebellum. The human cerebellum, cerebellar connections, and cerebellar cortex. Minneapolis: The University of Minnesota Press.
Leaton, R. N., & Supple, W. F., Jr. (1986). Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science, 232(4749), 513–515.
Lee, H., Sohn, S. I., Cho, Y. W., Lee, S. R., Ahn, B. H., Park, B. R., et al. (2006). Cerebellar infarction presenting isolated vertigo: frequency and vascular topographical patterns. Neurology, 67(7), 1178–1183.
Leggio, M. G., Chiricozzi, F. R., Clausi, S., Tedesco, A. M., & Molinari, M. (2009). The neuropsychological profile of cerebellar damage: The sequencing hypothesis. Cortex, Sep 6. [Epub ahead of print]
Leiner, H. C., Leiner, A. L., & Dow, R. S. (1986). Does the cerebellum contribute to mental skills? Behavioral Neuroscience, 100(4), 443–454.
Levinson, H. N. (1988). The cerebellar-vestibular basis of learning disabilities in children, adolescents and adults: hypothesis and study. Perceptual and Motor Skills, 67(3), 983–1006.
Levisohn, L., Cronin-Golomb, A., & Schmahmann, J. D. (2000). Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain, 123(Pt 5), 1041–1050.
Limperopoulos, C., Soul, J. S., Haidar, H., Huppi, P. S., Bassan, H., Warfield, S. K., et al. (2005). Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics, 116(4), 844–850.
Limperopoulos, C., Bassan, H., Gauvreau, K., Robertson, R. L., Jr., Sullivan, N. R., Benson, C. B., et al. (2007). Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics, 120(3), 584–593.
Locke, S. (1969). Modern neurology papers in tribute to Denny-Brown. Boston: Little Brown.
Maeshima, S., & Osawa, A. (2007). Stroke rehabilitation in a patient with cerebellar cognitive affective syndrome. Brain Injury, 21(8), 877–883.
Makris, N., Hodge, S. M., Haselgrove, C., Kennedy, D. N., Dale, A., Fischl, B., et al. (2003). Human cerebellum: surface-assisted cortical parcellation and volumetry with magnetic resonance imaging. Journal of Cognitive Neuroscience, 15(4), 584–599.
Makris, N., Schlerf, J. E., Hodge, S. M., Haselgrove, C., Albaugh, M. D., Seidman, L. J., et al. (2005). MRI-based surface-assisted parcellation of human cerebellar cortex: an anatomically specified method with estimate of reliability. Neuroimage, 25(4), 1146–1160.
Marr, D. (1969). A theory of cerebellar cortex. Journal de Physiologie, 202(2), 437–470.
Martner, J. (1975). Cerebellar influences on autonomic mechanisms. An experimental study in the cat with special reference to the fastigial nucleus. Acta Physiologica Scandinavica. Supplementum, 425, 1–42.
Mason, W. A., & Berkson, G. (1975). Effects of maternal mobility on the development of rocking and other behaviors in rhesus monkeys: a study with artificial mothers. Developmental Psychobiology, 8(3), 197–211.
May, J. G., & Andersen, R. A. (1986). Different patterns of corticopontine projections from separate cortical fields within the inferior parietal lobule and dorsal prelunate gyrus of the macaque. Experimental Brain Research, 63(2), 265–278.
Mayberg, H. S., Lozano, A. M., Voon, V., McNeely, H. E., Seminowicz, D., Hamani, C., et al. (2005). Deep brain stimulation for treatment-resistant depression. Neuron, 45(5), 651–660.
Mesulam, M. M. (1981). A cortical network for directed attention and unilateral neglect. Annals of Neurology, 10(4), 309–325.
Middleton, F. A., & Strick, P. L. (1994). Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science, 266(5184), 458–461.
Molinari, M., Leggio, M. G., Solida, A., Ciorra, R., Misciagna, S., Silveri, M. C., et al. (1997). Cerebellum and procedural learning: evidence from focal cerebellar lesions. Brain, 120(Pt 10), 1753–1762.
Molinari, M., Petrosini, L., Misciagna, S., & Leggio, M. G. (2004). Visuospatial abilities in cerebellar disorders. Journal of Neurology, Neurosurgery and Psychiatry, 75(2), 235–240.
Nadeau, S. E., & Crosson, B. (1997). Subcortical aphasia. Brain and Language, 58(3), 355–402. discussion 418–423.
Neau, J. P., Arroyo-Anllo, E., Bonnaud, V., Ingrand, P., & Gil, R. (2000). Neuropsychological disturbances in cerebellar infarcts. Acta Neurologica Scandinavica, 102(6), 363–370.
Neuburger, M. (1897/1981). Die historiche Entwicklung der experimentellen Gehirn-und Ruckenmarksphysiologie vor Flourens. Translated and edited, with additional material, by Edwin Clarke, as The Historical Development of Experimental Brain and Spinal Cord Physiology Before Flourens. Baltimore/London: Johns Hopkins University Press.
Nicolson, R. I., & Fawcett, A. J. (2005). Developmental dyslexia, learning and the cerebellum. Journal of Neural Transmission. Supplementum (69), 19–36.
Nicolson, R. I., Fawcett, A. J., & Dean, P. (2001). Developmental dyslexia: the cerebellar deficit hypothesis. Trends in Neurosciences, 24(9), 508–511.
Nopoulos, P. C., Ceilley, J. W., Gailis, E. A., & Andreasen, N. C. (1999). MRI volumetry of the vermis and the cerebellar hemispheres in men with schizophrenia. Biological Psychiatry, 46, 703–711.
Nyby, O., & Jansen, J. (1951). An experimental investigation of the corticopontine projection in macaca mulatta. Skrifter utgitt av det Norske Vedenskapsakademie Oslo. Mat Naturv Klasse, 3, 1–47.
O’Reilly, J. X., Beckmann, C. F., Tomassini, V., Ramnani, N., & Johansen-Berg, H. (2010). Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cerebral Cortex, 20(4), 953–965.
Oscarsson, O. (1965). Functional organization of the spino- and cuneocerebellar tracts. Physiological Reviews, 45, 495–522.
Parvizi, J., Joseph, J. T., Press, D., & Schmahmann, J. D. (2007). Pathological laughter and crying in patients with multiple system atrophy-cerebellar type. Movement Disorders, 22, 798–803.
Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M., & Raichle, M. E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature, 331(6157), 585–589.
Petrides, M., & Pandya, D. N. (1988). Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. The Journal of Comparative Neurology, 273(1), 52–66.
Petrosini, L., Molinari, M., & Dell’Anna, M. E. (1996). Cerebellar contribution to spatial event processing: Morris water maze and T-maze. The European Journal of Neuroscience, 8(9), 1882–1896.
Pollack, I. F., Polinko, P., Albright, A. L., Towbin, R., & Fitz, C. (1995). Mutism and pseudobulbar symptoms after resection of posterior fossa tumors in children: incidence and pathophysiology. Neurosurgery, 37(5), 885–893.
Prescott, J. W. (1971). Early somatosensory deprivation as ontogenic process in the abnormal development of the brain and behavior. In Moor-Jankowski EIGaJ (Ed.), Medical primatology 1970. Basel: Karger.
Rapoport, M., van Reekum, R., & Mayberg, H. (2000). The role of the cerebellum in cognition and behavior: a selective review. The Journal of Neuropsychiatry and Clinical Neurosciences, 12(2), 193–198.
Rauch, S. L., Dougherty, D. D., Malone, D., Rezai, A., Friehs, G., Fischman, A. J., et al. (2006). A functional neuroimaging investigation of deep brain stimulation in patients with obsessive-compulsive disorder. Journal of Neurosurgery, 104(4), 558–565.
Reynolds, D., & Nicolson, R. I. (2007). Follow-up of an exercise-based treatment for children with reading difficulties. Dyslexia, 13(2), 78–96.
Reynolds, D., Nicolson, R. I., & Hambly, H. (2003). Evaluation of an exercise-based treatment for children with reading difficulties. Dyslexia, 9(1), 48–71. discussion 46–47.
Richter, S., Aslan, B., Gerwig, M., Wilhelm, H., Kramer, S., Todica, O., et al. (2007). Patients with chronic focal cerebellar lesions show no cognitive abnormalities in a bedside test. Neurocase, 13(1), 25–36.
Riva, D., & Giorgi, C. (2000). The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain, 123(Pt 5), 1051–1061.
Sadeh, M., & Cohen, I. (2001). Transient loss of speech after removal of posterior fossa tumors—one aspect of a larger neuropsychological entity: the cerebellar cognitive affective syndrome. Pediatric Hematology and Oncology, 18(7), 423–426.
Sasaki, K., Oka, H., Matsuda, Y., Shimono, T., & Mizuno, N. (1975). Electrophysiological studies of the projections from the parietal association area to the cerebellar cortex. Experimental Brain Research, 23, 91–102.
Schmahmann, J. (1991). An emerging concept. The cerebellar contribution to higher function. Archives of Neurology, 48(11), 1178–1187.
Schmahmann, J. D. (1994). The cerebellum in autism: Clinical and anatomic perspectives. In M. L. Bauman & T. L. Kemper (Eds.), The neurobiology of autism (pp. 195–226). Baltimore: Johns Hopkins University Press.
Schmahmann, J. D. (1996). From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Human Brain Mapping, 4, 174–198.
Schmahmann, J. D. (1997a). The cerebellum and cognition. Int Rev Neurobiol, vol 41. San Diego: Academic.
Schmahmann, J. D. (1997b). Therapeutic and research implications. In J. D. Schmahmann (Ed.), The cerebellum and cognition. Int Rev Neurobiol, 41, 637–647. San Diego: Academic.
Schmahmann, J. D. (1998). Dysmetria of thought. Clinical consequences of cerebellar dysfunction on cognition and affect. Trends in Cognitive Sciences, 2, 362–370.
Schmahmann, J. D. (2000). The role of the cerebellum in affect and psychosis. Journal of Neurolinguistics, 13, 189–214.
Schmahmann, J. D. (2001). The cerebellar cognitive affective syndrome: clinical correlations of the dysmetria of thought hypothesis. International Review of Psychiatry, 13, 313–322.
Schmahmann, J. D. (2004). Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(3), 367–378.
Schmahmann, J. D., Doyon, J., McDonald, D., Holmes, C., Lavoie, K., Hurwitz, A. S., et al. (1999). Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage, 10(3 Pt 1), 233–260.
Schmahmann, J. D., Doyon, J., Toga, A., Evans, A., & Petrides, M. (2000). MRI atlas of the human cerebellum. San Diego: Academic.
Schmahmann, J. D., Gardner, R. C., MacMore, J., & Vangel, M. (2009b). Development of a brief ataxia rating scale (BARS) based on a modified form of the ICARS. Movement Disorders, 24, 1820–1828.
Schmahmann, J. D., Hurwitz, A. S., Loeber, R. T., & Marjani, J. L. (1998a). A semi-flattened map of the human cerebellum. A new approach to visualizing the cerebellar cortex in 2-dimensional space. Society for Neuroscience Abstracts, 24, 1409.
Schmahmann, J. D., Loeber, R. T., Marjani, J., & Hurwitz, A. S. (1998b). Topographic organization of cognitive functions in the human cerebellum. A meta-analysis of functional imaging studies. Neuroimage, 7, S721.
Schmahmann, J. D., MacMore, J., & Vangel, M. (2009a). Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience, 162(3), 852–861.
Schmahmann, J. D., & Pandya, D. N. (1987). Posterior parietal projections to the basis pontis in rhesus monkey. Possible anatomical substrate for the cerebellar modulation of complex behavior. Neurology, 37, 297.
Schmahmann, J. D., & Pandya, D. N. (1989). Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. The Journal of Comparative Neurology, 289(1), 53–73.
Schmahmann, J. D., & Pandya, D. N. (1990). Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: a WGA-HRP and fluorescent tracer study. The Journal of Comparative Neurology, 295(2), 299–326.
Schmahmann, J. D., & Pandya, D. N. (1991). Projections to the basis pontis from the superior temporal sulcus and superior temporal region in the rhesus monkey. The Journal of Comparative Neurology, 308(2), 224–248.
Schmahmann, J. D., & Pandya, D. N. (1992). Course of the fiber pathways to pons from parasensory association areas in the rhesus monkey. The Journal of Comparative Neurology, 326(2), 159–179.
Schmahmann, J. D., & Pandya, D. N. (1993). Prelunate, occipitotemporal, and parahippocampal projections to the basis pontis in rhesus monkey. The Journal of Comparative Neurology, 337(1), 94–112.
Schmahmann, J. D., & Pandya, D. N. (1995). Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neuroscience Letters, 199(3), 175–178.
Schmahmann, J. D., & Pandya, D. N. (1997a). Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. The Journal of Neuroscience, 17(1), 438–458.
Schmahmann, J. D., & Pandya, D. N. (1997b). The cerebrocerebellar system. In J. D. Schmahmann (Ed.), The cerebellum and cognition. Int Rev Neurobiol, 41, 31–60. San Diego: Academic.
Schmahmann, J. D., & Pandya, D. (2006). Fiber pathways of the brain. New York: Oxford University Press.
Schmahmann, J. D., & Pandya, D. N. (2008). Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex, 44(8), 1037–1066.
Schmahmann, J. D., & Sherman, J. C. (1997). Cerebellar cognitive affective syndrome. In J. D. Schmahmann (Ed.), The Cerebellum and Cognition. Int Rev Neurobiol, 41, 433–440. San Diego: Academic.
Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121(Pt 4), 561–579.
Schmahmann, J. D., Rosene, D. L., & Pandya, D. N. (2004). Motor projections to the basis pontis in rhesus monkey. The Journal of Comparative Neurology, 478(3), 248–268.
Schmahmann, J. D., Weilburg, J. B., & Sherman, J. C. (2007). The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum, 6(3), 254–267.
Schweizer, T. A., Levine, B., Rewilak, D., O’Connor, C., Turner, G., Alexander, M. P., et al. (2008). Rehabilitation of executive functioning after focal damage to the cerebellum. Neurorehabilitation and Neural Repair, 22(1), 72–77.
Seltzer, B., & Pandya, D. N. (1984). Further observations on parieto-temporal connections in the rhesus monkey. Experimental Brain Research, 55, 301–312.
Snider, R. S. (1950). Recent contributions to the anatomy and physiology of the cerebellum. Archives of Neurology and Psychiatry, 64(2), 196–219.
Snider, R. S. (1952). Interrelations of cerebellum and brainstem. Research Publications—Association for Research in Nervous and Mental Disease, 30, 267–281.
Snider, R. S., & Eldred, E. (1948). Cerebral projections to the tactile, auditory and visual areas of the cerebellum. The Anatomical Record, 100, 714.
Snider, R. S., & Maiti, A. (1976). Cerebellar contributions to the Papez circuit. Journal of Neuroscience Research, 2(2), 133–146.
Snider, R. S., & Stowell, A. (1944). Receiving areas of the tactile, auditory, and visual systems in the cerebellum. Journal of Neurophysiology, 7, 331–357.
Snider, S. R. (1982). Cerebellar pathology in schizophrenia—cause or consequence? Neuroscience and Biobehavioral Reviews, 6(1), 47–53.
Snowling, M. J., & Hulme, C. (2003). A critique of claims from Reynolds, Nicolson & Hambly (2003) that DDAT is an effective treatment for children with reading difficulties—‘lies, damned lies and (inappropriate) statistics’? Dyslexia, 9(2), 127–133. discussion 134–125.
Steinlin, M., Imfeld, S., Zulauf, P., Boltshauser, E., Lovblad, K. O., Ridolfi Luthy, A., et al. (2003). Neuropsychological long-term sequelae after posterior fossa tumour resection during childhood. Brain, 126(Pt 9), 1998–2008.
Stoodley, C. J., & Schmahmann, J. D. (2009). Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage, 44(2), 489–501.
Stoodley, C. J., & Schmahmann, J. D. (2010). Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex, 46(7), 831–844.
Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2010a). An fMRI case study of functional topography in the human cerebellum. Behavioural Neurology, 23(1), 65–79.
Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2010b). Functional topography in the cerebellum for motor and cognitive tasks: An fMRI study. Society for Neuroscience, 2010. Online.
Strick, P. L., Dum, R. P., & Fiez, J. A. (2009). Cerebellum and nonmotor function. Annual Review of Neuroscience, 32, 413–434.
Sugihara, I., & Shinoda, Y. (2004). Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. The Journal of Neuroscience, 24(40), 8771–8785.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. 3-Dimensional proportional system: An approach to cerebral imaging (Translated by Mark Rayport.). New York: Thieme.
Tavano, A., Grasso, R., Gagliardi, C., Triulzi, F., Bresolin, N., Fabbro, F., et al. (2007). Disorders of cognitive and affective development in cerebellar malformations. Brain, 130(Pt 10), 2646–2660.
Thach, W. T. (1987). Cerebellar inputs to motor cortex. Ciba Foundation Symposium, 132, 201–220.
Thompson, R. F. (1983). Neuronal substrate of simple associative learning. Classical conditioning. Trends in Neurosciences, 6, 270–275.
Timmann, D., Brandauer, B., Hermsdorfer, J., Ilg, W., Konczak, J., Gerwig, M., et al. (2008). Lesion-symptom mapping of the human cerebellum. Cerebellum, 7(4), 602–606.
Timmann, D., Drepper, J., Frings, M., Maschke, M., Richter, S., Gerwig, M., et al. (2010). The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex, 46(7), 845–857.
Trouillas, P., Takayanagi, T., Hallett, M., Currier, R. D., Subramony, S. H., Wessel, K., et al. (1997). International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharmacology Committee of the World Federation of Neurology. Journal of the Neurological Sciences, 145(2), 205–211.
Turkeltaub, P. E., Eden, G. F., Jones, K. M., & Zeffiro, T. A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage, 16, 765–780.
Valenstein, E., Heilman, K. M., Watson, R. T., & Van Den Abell, T. (1982). Nonsensory neglect from parietotemporal lesions in monkeys. Neurology, 32(10), 1198–1201.
Vilensky, J., & van Hoesen, G. V. (1981). Corticopontine projections from the cingulate cortex in the rhesus monkey. Brain Research, 205, 391–395.
Voogd, J. (2004). Cerebellum and precerebellar nuclei. In G. Paxinos & J. Mai (Eds.), The human nervous system (pp. 321–392). San Diego: Academic.
Voogd, J., & Glickstein, M. (1998). The anatomy of the cerebellum. Trends in Neurosciences, 21(9), 370–375.
Watson, P. J. (1978). Nonmotor functions of the cerebellum. Psychological Bulletin, 85(5), 944–967.
Watson, R. T., Valenstein, E., & Heilman, K. M. (1981). Thalamic neglect. Possible role of the medial thalamus and nucleus reticularis in behavior. Archives of Neurology, 38(8), 501–506.
Weinberger, D. R., Kleinman, J. E., Luchins, D. J., Bigelow, L. B., & Wyatt, R. J. (1980). Cerebellar pathology in schizophrenia: a controlled postmortem study. The American Journal of Psychiatry, 137(3), 359–361.
Whitney, E. R., Kemper, T. L., Rosene, D. L., Bauman, M. L., & Blatt, G. J. (2009). Density of cerebellar basket and stellate cells in autism: evidence for a late developmental loss of Purkinje cells. Journal of Neuroscience Research, 87(10), 2245–2254.
Wiesendanger, R., Wiesendanger, M., & Ruegg, D. G. (1979). An anatomical investigation of the corticopontaine projection in the primate (Macaca fascicularis and Saimiri sciureus)-II. The projection from frontal and parental association areas. Neuroscience, 4(6), 747–765.
Wisoff, J. H., & Epstein, F. J. (1984). Pseudobulbar palsy after posterior fossa operation in children. Neurosurgery, 15(5), 707–709.
Wolf, J. K. (1971). The classical brainstem syndromes. Springfield: Charles C. Thomas.
Woolsey, C. N. (1952). Summary of the papers on the cerebellum. Research Publications—Association for Research in Nervous and Mental Disease, 30, 334–336.
Yeterian, E. H., & Van Hoesen, G. W. (1978). Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Research, 139(1), 43–63.
Zanchetti, A., & Zoccolini, A. (1954). Autonomic hypothalamic outbursts elicited by cerebellar stimulation. Journal of Neurophysiology, 17(5), 475–483.
Acknowledgements
Supported in part by NIH R01 MH067980, the Sidney R. Baer Jr Foundation, the MINDlink Foundation, the Birmingham Foundation, and the Massachusetts General Hospital Executive Committee on Research. The assistance of Jinny Sagorin, Jason MacMore and Laura Horton is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schmahmann, J.D. 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 20, 236–260 (2010). https://doi.org/10.1007/s11065-010-9142-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11065-010-9142-x