Cerebellar neurocognition: Insights into the bottom of the brain

The traditional view on the core functions of the cerebellum consists of the regulation of motor coordination, balance and motor speech. However, during the past decades results from neuroanatomical, neuroimaging and clinical studies have substantially extended the functional role of the cerebellum to cognitive and affective regulation. Neuroanatomical studies convincingly showed cerebellar connectivity with associative areas of the cerebral cortex involved in higher cognitive functioning, while functional neuroimaging provided evidence of cerebellar activation during a variety of cognitive tasks. In addition, more systematic neuropsychological research performed in patients with cerebellar lesions and the development of more sensitive neuropsychological tests allowed clinicians to identify significant cognitive and affective disturbances following cerebellar damage. In this review, an overview is presented of the cerebellar role in a variety of cognitive processes, such as executive functioning, memory, learning, attention, visuo-spatial regulation, language and behavioral-affective modulation. In addition, recent evidence with regard to cerebellar induced clinical entities such as the cerebellar cognitive affective syndrome (CCAS) and the posterior fossa syndrome (PFS), will be discussed. Although extensive research has substantially broadened the insights in the cognitive and affective role of the cerebellum, the precise nature of the cerebellar contribution to cognitive and affective regulation is not yet clear. In this review experimental and clinical data will be discussed that substantiate the presumed neurobiological mechanisms underlying the cognitive and affective modulatory role of the cerebellum.

[1]  Gereon R. Fink,et al.  Using fMRI to decompose the neural processes underlying the Wisconsin Card Sorting Test , 2006, NeuroImage.

[2]  S. Waga,et al.  Mutism after removal of a vermian medulloblastoma: cerebellar mutism. , 1991, Surgical neurology.

[3]  R. Kawashima,et al.  Human cerebellum plays an important role in memory-timed finger movement: an fMRI study. , 2000, Journal of neurophysiology.

[4]  Matti Laine,et al.  Naming of newly learned objects: a PET activation study. , 2005, Brain research. Cognitive brain research.

[5]  J. Piatt,et al.  Resection of fourth ventricle tumors without splitting the vermis: the cerebellomedullary fissure approach. , 1997, Pediatric neurosurgery.

[6]  M. Molinari,et al.  The cerebellum contributes to linguistic production , 1994, Neurology.

[7]  A. Luxen,et al.  Involvement of both prefrontal and inferior parietal cortex in dual-task performance. , 2005, Brain research. Cognitive brain research.

[8]  M. Molinari,et al.  Cerebellum and procedural learning: evidence from focal cerebellar lesions. , 1997, Brain : a journal of neurology.

[9]  Ü. Yararbaş,et al.  Single photon emission tomography following posterior fossa surgery in patients with and without mutism , 2002, Child's Nervous System.

[10]  J. Plese,et al.  Transient mutism following a posterior fossa approach to cerebellar tumors in children: a critical review of the literature , 1995, Child's Nervous System.

[11]  F Barkhof,et al.  Visualizing brain activation during planning: the tower of London test adapted for functional MR imaging. , 2000, AJNR. American journal of neuroradiology.

[12]  Julie A Fiez,et al.  Cerebellar damage produces selective deficits in verbal working memory. , 2006, Brain : a journal of neurology.

[13]  P. Watson Nonmotor functions of the cerebellum. , 1978, Psychological bulletin.

[14]  Julie A. Fiez,et al.  Cerebellar contributions to verbal working memory: beyond cognitive theory , 2008, The Cerebellum.

[15]  K. Krishnan,et al.  Volumetric brain imaging findings in mood disorders. , 2002, Bipolar disorders.

[16]  S. Paradiso,et al.  The cerebellum and emotional experience , 2007, Neuropsychologia.

[17]  B. Sheikh,et al.  Cerebellar mutism caused by arteriovenous malformation of the vermis. , 2001, British journal of neurosurgery.

[18]  John E. Desmond,et al.  Cerebellar involvement in cognitive function: evidence from neuroimaging , 2001 .

[19]  A. Swann,et al.  Chronic exposure to MDMA (Ecstasy) elicits behavioral sensitization in rats but fails to induce cross-sensitization to other psychostimulants. , 2006, Behavioral and brain functions : BBF.

[20]  W. James,et al.  Il Cervelletto. Nuovi Studi di Fisiologia Normale e Patologica. , 1893 .

[21]  Chetwyn C. H. Chan,et al.  The cerebellum's involvement in the judgment of spatial orientation: A functional magnetic resonance imaging study , 2005, Neuropsychologia.

[22]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[23]  T. Yagi,et al.  A NEW NEUROTOLOGICAL TEST FOR DETECTING CEREBELLAR DYSFUNCTION , 1981, Annals of the New York Academy of Sciences.

[24]  Boris Suchan,et al.  Cortico-subcortical contributions to executive control. , 2004, Acta psychologica.

[25]  Richard B. Ivry,et al.  The cognitive neuropsychology of the cerebellum , 2001 .

[26]  G. Logan Executive control of thought and action , 1985 .

[27]  Michiyasu Suzuki,et al.  Mutism after evacuation of acute subdural hematoma of the posterior fossa , 2005, Child's Nervous System.

[28]  M. Pinsk,et al.  Functional Localization of a “Time Keeper” Function Separate from Attentional Resources and Task Strategy , 2000, NeuroImage.

[29]  S. Pomeroy,et al.  Neurological Dysfunction Associated With Postoperative Cerebellar Mutism , 2000, Journal of Neuro-Oncology.

[30]  Bruce E. Murdoch,et al.  Higher‐level language deficits resulting from left primary cerebellar lesions , 2004 .

[31]  R. Luerding,et al.  Impaired working-memory after cerebellar infarcts paralleled by changes in BOLD signal of a cortico-cerebellar circuit , 2007, Neuropsychologia.

[32]  Peter Thier,et al.  Disturbed overt but normal covert shifts of attention in adult cerebellar patients. , 2005, Brain : a journal of neurology.

[33]  M. Silveri,et al.  Right side neglect in right cerebellar lesion , 2001, Journal of neurology, neurosurgery, and psychiatry.

[34]  J. Ross,et al.  The mind's eye: functional MR imaging evaluation of golf motor imagery. , 2003, AJNR. American journal of neuroradiology.

[35]  Timothy Justus The Cerebellum and English Grammatical Morphology: Evidence from Production, Comprehension, and Grammaticality Judgments , 2004, Journal of Cognitive Neuroscience.

[36]  J. Schmahmann,et al.  Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. , 2000, Brain : a journal of neurology.

[37]  J. Fiez,et al.  Functional heterogeneity within Broca's area during verbal working memory , 2002, Physiology & Behavior.

[38]  R. Likert “Technique for the Measurement of Attitudes, A” , 2022, The SAGE Encyclopedia of Research Design.

[39]  M. Jüptner,et al.  Localization of a cerebellar timing process using PET , 1995, Neurology.

[40]  K W Greve,et al.  Cognitive and emotional sequelae of cerebellar infarct: a case report. , 1999, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[41]  D. Stuss,et al.  Rehabilitation of Executive Functioning After Focal Damage to the Cerebellum , 2008, Neurorehabilitation and neural repair.

[42]  M. Molinari,et al.  Verbal short-term store-rehearsal system and the cerebellum. Evidence from a patient with a right cerebellar lesion. , 1998, Brain : a journal of neurology.

[43]  F. Sklar,et al.  Posterior Fossa Syndrome: Identifiable Risk Factors and Irreversible Complications , 1999, Pediatric Neurosurgery.

[44]  R. J. Frank,et al.  Reliability of PET activation across statistical methods, subject groups, and sample sizes , 1996, Human brain mapping.

[45]  D. Riva,et al.  The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. , 2000, Brain : a journal of neurology.

[46]  V. Calhoun,et al.  Functional neural circuits for mental timekeeping , 2007, Human brain mapping.

[47]  B. Mazoyer,et al.  A Common Language Network for Comprehension and Production: A Contribution to the Definition of Language Epicenters with PET , 2000, NeuroImage.

[48]  Catherine J. Stoodley,et al.  Lateralized cognitive deficits in children following cerebellar lesions , 2001, Developmental medicine and child neurology.

[49]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[50]  S. Petersen,et al.  Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. , 1992, Brain : a journal of neurology.

[51]  Yoshiro Okubo,et al.  Reduced volume of the cerebellar vermis in neuroleptic-naive schizophrenia , 2001, Biological Psychiatry.

[52]  Wolfram Ziegler,et al.  Cognitive functions in patients with MR-defined chronic focal cerebellar lesions , 2007, Journal of Neurology.

[53]  Hubertus Maximilian Mehdorn,et al.  Does the cerebellum contribute to specific aspects of attention? , 2003, Neuropsychologia.

[54]  J Townsend,et al.  Impairment in shifting attention in autistic and cerebellar patients. , 1994, Behavioral neuroscience.

[55]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[56]  J. Schmahmann,et al.  The neuropsychiatry of the cerebellum — insights from the clinic , 2008, The Cerebellum.

[57]  P. Deyn,et al.  Cognitive, linguistic and affective disturbances following a right superior cerebellar artery infarction: A case study , 2009, Cortex.

[58]  Four cases of Friedreich's ataxia: with a critical review of recent literature on the subject , 1898 .

[59]  R. Dow,et al.  The Physiology and Pathology of the Cerebellum , 1958 .

[60]  Christian Bellebaum,et al.  Cerebellar involvement in executive control , 2008, The Cerebellum.

[61]  Robert Lalonde,et al.  Neuropsychological deficits of patients with chronic or acute cerebellar lesions , 2000, Journal of Neurolinguistics.

[62]  N. Birbaumer,et al.  The cerebellum and cognitive functions in humans. , 1993, Behavioral neuroscience.

[63]  E. Moens,et al.  Cerebellar induced aphasia: case report of cerebellar induced prefrontal aphasic language phenomena supported by SPECT findings , 1996, Journal of the Neurological Sciences.

[64]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[65]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[66]  A. Georgopoulos,et al.  Functional magnetic resonance imaging of mental rotation and memory scanning: a multidimensional scaling analysis of brain activation patterns 1 Published on the World Wide Web on 24 February 1998. 1 , 1998, Brain Research Reviews.

[67]  R. Ivry,et al.  Impaired Velocity Perception in Patients with Lesions of the Cerebellum , 1991, Journal of Cognitive Neuroscience.

[68]  G. Drost,et al.  Cerebellar Involvement as a Rare Complication of Pneumococcal Meningitis , 2000, Neuropediatrics.

[69]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[70]  H. Diener,et al.  On the neural basis of focused and divided attention. , 2005, Brain research. Cognitive brain research.

[71]  P. Ingrand,et al.  Neuropsychological disturbances in cerebellar infarcts , 2000, Acta neurologica Scandinavica.

[72]  A. L. Leiner,et al.  Does the cerebellum contribute to mental skills? , 1986, Behavioral neuroscience.

[73]  Godehard Weniger,et al.  Cerebellar lesions in the PICA but not SCA territory impair cognition , 2004, Neurology.

[74]  J. Bower,et al.  Involvement of the cerebellum in semantic discrimination: An fMRI study , 2003, Human brain mapping.

[75]  B. Dan,et al.  Nonsurgical cerebellar mutism (anarthria) in two children. , 2003, Pediatric neurology.

[76]  P. Chapman,et al.  Concepts in pediatric neurosurgery , 1981 .

[77]  J Drepper,et al.  Non-motor associative learning in patients with isolated degenerative cerebellar disease. , 1999, Brain : a journal of neurology.

[78]  C A Meyers,et al.  Postoperative mutism in neurosurgery. Report of two cases. , 1994, Journal of neurosurgery.

[79]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[80]  B. Schoch,et al.  Cerebellar mutism , 2004, Brain and Language.

[81]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[82]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[83]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[84]  P. Paquier,et al.  Tumour type and size are high risk factors for the syndrome of “cerebellar” mutism and subsequent dysarthria , 1999, Journal of neurology, neurosurgery, and psychiatry.

[85]  I. Aiello,et al.  Pure post–stroke cerebellar cognitive affective syndrome: a case report , 2004, Neurological Sciences.

[86]  O Salonen,et al.  Subtle cognitive deficits after cerebellar infarcts , 2006, European journal of neurology.

[87]  Masao Ito Long-term depression as a memory process in the cerebellum , 1986, Neuroscience Research.

[88]  Alan C. Evans,et al.  Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction , 1998, Journal of Cognitive Neuroscience.

[89]  M G Leggio,et al.  Visuospatial abilities in cerebellar disorders , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[90]  Mutism and cerebellar dysarthria after brain stem surgery: case report. , 1995 .

[91]  J. Schmahmann Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[92]  Albert Gjedde,et al.  Putative Tests of Frontal Lobe Function: A PET-Study of Brain Activation During Stroop's Test and Verbal Fluency , 2002, Journal of clinical and experimental neuropsychology.

[93]  Peter Thier,et al.  The attentive cerebellum — myth or reality? , 2008, The Cerebellum.

[94]  Stefano F. Cappa,et al.  Agrammatic speech production after a right cerebellar haemorrhage , 1997 .

[95]  P. Deyn,et al.  Neurobehavioral alterations in an adolescent following posterior fossa tumor resection , 2008, The Cerebellum.

[96]  Amy J Bastian,et al.  Cerebellar damage impairs automaticity of a recently practiced movement. , 2002, Journal of neurophysiology.

[97]  C. Koch,et al.  Brain Areas Specific for Attentional Load in a Motion-Tracking Task , 2001, Journal of Cognitive Neuroscience.

[98]  J. Massion,et al.  Cerebro-cerebellar interactions , 1979 .

[99]  P. Paquier,et al.  Postoperative motor speech production in children with the syndrome of 'cerebellar' mutism and subsequent dysarthria: a critical review of the literature. , 2007, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[100]  Richard B. Ivry,et al.  Cerebellar activation during discrete and not continuous timed movements: An fMRI study , 2007, NeuroImage.

[101]  C. Catsman-Berrevoets,et al.  Transient Loss of Speech Followed by Dysarthria after Removal of Posterior Fossa Tumour , 1992, Developmental medicine and child neurology.

[102]  R. Bunge,et al.  Clinical use of frozen semen: report of four cases. , 1954, Fertility and sterility.

[103]  I. Pollack,et al.  Posterior fossa syndrome. , 1997, International review of neurobiology.

[104]  D. Woodruff-Pak,et al.  Huntington's disease and eyeblink classical conditioning: Normal learning but abnormal timing , 1996, Journal of the International Neuropsychological Society.

[105]  H. Mehdorn,et al.  Evidence for distinct cognitive deficits after focal cerebellar lesions , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[106]  S. Engelborghs,et al.  Cerebellar neurocognition: a new avenue. , 2001, Acta neurologica Belgica.

[107]  N. Korsakova,et al.  Cognitive Impairments in Cerebellar Infarcts , 2005, Neuroscience and Behavioral Physiology.

[108]  M. Sarter,et al.  The cognitive neuroscience of sustained attention: where top-down meets bottom-up , 2001, Brain Research Reviews.

[109]  M. Hallett,et al.  Memory in patients with cerebellar degeneration , 1993, Neurology.

[110]  Jordan Grafman,et al.  Perceptual timing in cerebellar degeneration , 1996, Neuropsychologia.

[111]  J. Schmahmann,et al.  The cerebellar cognitive affective syndrome. , 1998, Brain : a journal of neurology.

[112]  Sebastiaan Engelborghs,et al.  Aphasia following cerebellar damage: fact or fallacy? , 2000, Journal of Neurolinguistics.

[113]  M. Berger,et al.  The pathophysiology of oral pharyngeal apraxia and mutism following posterior fossa tumor resection in children. , 1995, Journal of neurosurgery.

[114]  D. Haines,et al.  Clinical symptoms of cerebellar disease and their interpretation , 2008, The Cerebellum.

[115]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[116]  Eric Courchesne,et al.  ERP Evidence for a Shifting Attention Deficit in Patients with Damage to the Cerebellum , 1994, Journal of Cognitive Neuroscience.

[117]  P. Deyn,et al.  The Lateralized Linguistic Cerebellum: A Review and a New Hypothesis , 2001, Brain and Language.

[118]  M. Botez,et al.  Neuropsychological Functioning in Unilateral Cerebellar Damage , 1994, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[119]  Y. Erşahin,et al.  Cerebellar mutism: report of two unusual cases and review of the literature , 1997, Clinical Neurology and Neurosurgery.

[120]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[121]  M. Chafetz,et al.  The cerebellum and cognitive function: implications for rehabilitation. , 1996, Archives of physical medicine and rehabilitation.

[122]  G. A. Clark,et al.  The engram found? Role of the cerebellum in classical conditioning of nictitating membrane and eyelid responses , 1981 .

[123]  Carlos M. Gómez,et al.  Behavioral and Brain Functions , 2006 .

[124]  Hiroshi Ito,et al.  Transient mutism after posterior fossa surgery , 1994, Child's Nervous System.

[125]  J. Moll,et al.  Functional MRI correlates of real and imagined tool-use pantomimes , 2000, Neurology.

[126]  Markus Frings,et al.  Cerebellar involvement in verb generation: An fMRI study , 2006, Neuroscience Letters.

[127]  R. Hales,et al.  J Neuropsychiatry Clin Neurosci , 1992 .

[128]  S. Corti,et al.  Long-term neuropsychological deficits after cerebellar infarctions in two young adult twins , 2004, Neuropsychologia.

[129]  P. Paquier,et al.  Posterior Fossa Syndrome after a Vermian Stroke: A New Case and Review of the Literature , 2007, Pediatric Neurosurgery.

[130]  V Bracha,et al.  Patients with cerebellar lesions cannot acquire but are able to retain conditioned eyeblink reflexes. , 1997, Brain : a journal of neurology.

[131]  M Dennis,et al.  Perception and estimation of time in long-term survivors of childhood posterior fossa tumors , 2000, Journal of the International Neuropsychological Society.

[132]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[133]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.