Cognitive sequencing impairment in patients with focal or atrophic cerebellar damage.

Although cognitive impairment after cerebellar damage has been widely reported, the mechanisms of cerebro-cerebellar interactions are still a matter of debate. The cerebellum is involved in sequence detection and production in both motor and sensory domains, and sequencing has been proposed as the basic mechanism of cerebellar functioning. Furthermore, it has been suggested that knowledge of sequencing mechanisms may help to define cerebellar predictive control processes. In spite of its recognized importance, cerebellar sequencing has seldom been investigated in cognitive domains. Cognitive sequencing functions are often analysed by means of action/script elaboration. Lesion and activation studies have localized this function in frontal cortex and basal ganglia circuits. The present study is the first to report deficits in script sequencing after cerebellar damage. We employed a card-sequencing test, developed ad hoc, to evaluate the influence of the content to be sequenced. Stimuli consisted of sets of sentences that described actions with a precise logical and temporal sequence (Verbal Factor), sets of cartoon-like drawings that reproduced behavioural sequences (Behavioural Factor) or abstract figures (Spatial Factor). The influence of the lesion characteristics was analysed by grouping patients according to lesion-type (focal or atrophic) and lesion-side (right or left). The results indicated that patients with cerebellar damage present a cognitive sequencing impairment independently of lesion type or localization. A correlation was also shown between lesion side and characteristics of the material to be sequenced. Namely, patients with left lesions perform defectively only on script sequences based on pictorial material and patients with right lesions only on script sequences requiring verbal elaboration. The present data support the hypothesis that sequence processing is the cerebellar mode of operation also in the cognitive domain. In addition, the presence of right/left and pictorial/verbal differences is in agreement with the idea that cerebro-cerebellar interactions are organized in segregated cortico-cerebellar loops in which specificity is not related to the mode of functioning, but to the characteristics of the information processed.

[1]  James M Bower,et al.  Rethinking the "lesser brain". , 2003, Scientific American.

[2]  J M Bower,et al.  Control of sensory data acquisition. , 1997, International review of neurobiology.

[3]  J. Doyon,et al.  Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements , 1998, Neuropsychologia.

[4]  Philip M. Corsi Human memory and the medial temporal region of the brain. , 1972 .

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

[6]  D. Pandya,et al.  The cerebrocerebellar system. , 1997, International review of neurobiology.

[7]  Antonio Cerasa,et al.  Sensorimotor transduction of time information is preserved in subjects with cerebellar damage , 2005, Brain Research Bulletin.

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

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

[10]  L Mandolesi,et al.  Learning power of single behavioral units in acquisition of a complex spatial behavior: an observational learning study in cerebellar-lesioned rats. , 2002, Behavioral neuroscience.

[11]  Masao Ito Bases and implications of learning in the cerebellum--adaptive control and internal model mechanism. , 2005, Progress in brain research.

[12]  Tanaka The role of , 2000, Journal of insect physiology.

[13]  Orsini Arturo,et al.  WAIS-R. Contributo alla taratura italiana , 1998 .

[14]  V. Lovelace-Chandler The Cerebellum and the Adaptive Coordination of Movement. Thach WT, Goodkin HP, Keating JG. Ann Rev Neurosci 15:403-442, 1992. , 1993 .

[15]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[16]  Arthur L. Benton,et al.  Word fluency and brain damage , 1967 .

[17]  Masao Ito Cerebellar circuitry as a neuronal machine , 2006, Progress in Neurobiology.

[18]  Chantal E. Stern,et al.  Fronto-striatal deficit in Parkinson's disease during semantic event sequencing , 2008, Neurobiology of Aging.

[19]  H. Diener,et al.  Learning of sensory sequences in cerebellar patients. , 2004, Learning & memory.

[20]  J. Karhu,et al.  Anticipatory cerebellar responses during somatosensory omission in man , 2000, Human brain mapping.

[21]  L Mandolesi,et al.  Representation of actions in rats: the role of cerebellum in learning spatial performances by observation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Á. Pascual-Leone,et al.  Effect of focal cerebellar lesions on procedural learning in the serial reaction time task , 1998, Experimental Brain Research.

[23]  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.

[24]  M. Mauk,et al.  Cerebellar function: Coordination, learning or timing? , 2000, Current Biology.

[25]  A. Dimitrova,et al.  Stimulus-response versus stimulus-stimulus-response learning in cerebellar patients , 2004, Experimental Brain Research.

[26]  Markus Schwaiger,et al.  A H2 15O Positron Emission Tomography Study on Mental Imagery of Movement Sequences—The Effect of Modulating Sequence Length and Direction , 2002, NeuroImage.

[27]  R Ivry,et al.  Exploring the role of the cerebellum in sensory anticipation and timing: Commentary on Tesche and Karhu , 2000, Human brain mapping.

[28]  C. Caltagirone,et al.  Constructional Apraxia in Left Brain-Damaged Patients: A Planning Disorder? , 1977, Cortex.

[29]  M. E. Olvera-Cortés,et al.  Bilateral lesion of the cerebellar–dentate nucleus impairs egocentric sequential learning but not egocentric navigation in the rat , 2004, Neurobiology of Learning and Memory.

[30]  Stephen M. Rao,et al.  Distinct neural systems underlie learning visuomotor and spatial representations of motor skills , 2005, Human brain mapping.

[31]  M. Molinari,et al.  The cerebellum in the spatial problem solving: a co-star or a guest star? , 1998, Progress in Neurobiology.

[32]  G. M. Reicher,et al.  Clustering in free recall as a function of certain methodological variations. , 1966, Journal of experimental psychology.

[33]  R. Ivry Cerebellar timing systems. , 1997, International review of neurobiology.

[34]  Richard B. Ivry,et al.  Spatial and Temporal Sequence Learning in Patients with Parkinson's Disease or Cerebellar Lesions , 2003, Journal of Cognitive Neuroscience.

[35]  M. Molinari,et al.  Phonological grouping is specifically affected in cerebellar patients: a verbal fluency study , 2000, Journal of neurology, neurosurgery, and psychiatry.

[36]  P. Strick,et al.  Basal Ganglia Output and Cognition: Evidence from Anatomical, Behavioral, and Clinical Studies , 2000, Brain and Cognition.

[37]  J. Ashe,et al.  Cerebellum Activation Associated with Performance Change but Not Motor Learning , 2002, Science.

[38]  P. Nixon,et al.  The role of the cerebellum in preparing responses to predictable sensory events , 2008, The Cerebellum.

[39]  C. Marra,et al.  Double Dissociation Between Temporal and Spatial Pattern Processing in Patients with Frontal and Parietal Damage , 1990, Cortex.

[40]  A. Graziano,et al.  Cerebellar contribution to spatial event processing: characterization of procedural learning , 1999, Experimental Brain Research.

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

[42]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[43]  A. Sirigu,et al.  Distinct Frontal Regions for Processing Sentence Syntax and Story Grammar , 1998, Cortex.

[44]  Marco Molinari,et al.  Cerebellar input to the posterior parietal cortex in the rat , 2002, Brain Research Bulletin.

[45]  Domenico Restuccia,et al.  Cerebellar damage impairs detection of somatosensory input changes. A somatosensory mismatch-negativity study. , 2006, Brain : a journal of neurology.

[46]  H. Diener,et al.  Use of sequence information in associative learning in control subjects and cerebellar patients , 2008, The Cerebellum.

[47]  T. Shallice,et al.  Action Sequencing Deficit Following Frontal Lobe Lesion , 2002, Neurocase.

[48]  A. Sirigu,et al.  Deficit in Evaluating Pre-Determinated Sequences of Script Events in Patients with Parkinson's Disease , 1998, Cortex.

[49]  M. Hallett,et al.  Procedural learning in Parkinson's disease and cerebellar degeneration , 1993, Annals of neurology.

[50]  M. Molinari,et al.  Neuronal plasticity of interrelated cerebellar and cortical networks , 2002, Neuroscience.

[51]  P. Rubé,et al.  L’examen Clinique en Psychologie , 1959 .

[52]  R. Ivry,et al.  Temporal organization of "internal speech" as a basis for cerebellar modulation of cognitive functions. , 2004, Behavioral and cognitive neuroscience reviews.

[53]  C. Caltagirone,et al.  The Mental Deterioration Battery: Normative Data, Diagnostic Reliability and Qualitative Analyses of Cognitive Impairment , 1996 .

[54]  H. Diener,et al.  Acquisition of simple auditory and visual sequences in cerebellar patients , 2008, The Cerebellum.

[55]  Irene Daum,et al.  Cerebellar contributions to cognitive functions: A progress report after two decades of research , 2008, The Cerebellum.

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

[57]  V. Braitenberg,et al.  The detection and generation of sequences as a key to cerebellar function: Experiments and theory , 1997, Behavioral and Brain Sciences.

[58]  Chantal E. Stern,et al.  Evidence for the importance of basal ganglia output nuclei in semantic event sequencing: An fMRI study , 2006, Brain Research.

[59]  Richard lvry,et al.  Cerebellar timing systems. , 1997 .