Rule-Based Category Learning is Impaired in Patients with Parkinson's Disease but not in Patients with Cerebellar Disorders

The basal ganglia and cerebellum have both been implicated in motor skill acquisition. Recent hypotheses concerning cognitive functions of the basal ganglia and cerebellum have emphasized that these subcortical structures may also contribute to nonmotor learning. To explore this issue, patients with Parkinson's disease (PD) and patients with cerebellar lesions (CB) were tested on two category-learning tasks. Identical stimulus displays were used for the two tasks, consisting of a reference line and target line. In the length task, the two categories were defined based on the length of the target line. In the distance task, the two categories were defined by the distance between the target and reference lines. Thus, both categories could be defined by a simple rule in which attention must be restricted to a single relevant dimension. Consistent with previous results, the patients with PD were impaired on both tasks compared with neurologically healthy controls. In contrast, the CB patients performed similar to the control participants. Model-based analyses indicate that the patients with PD were able to select the appropriate categorization rule, but that they adopted suboptimal category boundaries in both conditions and were more variable in the application of the selected rule. These results provide an important neuropsychological dissociation on a non-motor-learning task between the effects of basal ganglia and cerebellar lesions. Moreover, the modeling work suggests that at least part of the Parkinson patients' impairment on these tasks reflect a tendency to exhibit strong response biases.

[1]  M. Horstink,et al.  Cognitive and motor shifting aptitude disorder in Parkinson's disease. , 1984, Journal of neurology, neurosurgery, and psychiatry.

[2]  Richard B. Ivry,et al.  Cerebellar and basal ganglia contributions to interval timing , 2003 .

[3]  J. Wickens A Theory of the Striatum , 1993 .

[4]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[5]  R B Ivry,et al.  Preserved performance by cerebellar patients on tests of word generation, discrimination learning, and attention. , 1997, Learning & memory.

[6]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[7]  Scott T Grafton,et al.  Cerebellar Involvement in Response Reassignment Rather Than Attention , 2002, The Journal of Neuroscience.

[8]  W. T. Maddox,et al.  Dissociating explicit and procedural-learning based systems of perceptual category learning , 2004, Behavioural Processes.

[9]  N. Hogan,et al.  Procedural motor learning in Parkinson's disease , 2001, Experimental Brain Research.

[10]  W. T. Thach,et al.  Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. , 1996, Brain : a journal of neurology.

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

[12]  Carol A. Seger,et al.  Striatal activation during acquisition of a cognitive skill. , 1999, Neuropsychology.

[13]  W. T. Maddox,et al.  Striatal contributions to category learning: Quantitative modeling of simple linear and complex nonlinear rule learning in patients with Parkinson's disease , 2001, Journal of the International Neuropsychological Society.

[14]  Paul Van Hecke,et al.  Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback , 2003, NeuroImage.

[15]  N. Gordon The cerebellum and cognition. , 2007, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[16]  W. Schultz Activity of dopamine neurons in the behaving primate , 1992 .

[17]  W. T. Maddox,et al.  Characterizing rule-based category learning deficits in patients with Parkinson's disease , 2007, Neuropsychologia.

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

[19]  C. Marsden,et al.  Recent Developments in Parkinson's Disease , 1986 .

[20]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[21]  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.

[22]  D. Harrington,et al.  Cognitive-motor learning in Parkinson's disease. , 1997, Neuropsychology.

[23]  Amanda Price Explicit category learning in Parkinson's disease: deficits related to impaired rule generation and selection processes. , 2006, Neuropsychology.

[24]  A. Pickering,et al.  New approaches to the study of amnesic patients: what can a neurofunctional philosophy and neural network methods offer? , 1997, Memory.

[25]  A. Canavan,et al.  Conditional associative learning is impaired in cerebellar disease in humans. , 1994, Behavioral neuroscience.

[26]  W Todd Maddox,et al.  Disrupting feedback processing interferes with rule-based but not information-integration category learning , 2004, Memory & cognition.

[27]  M. Hallett,et al.  Motor learning in patients with cerebellar dysfunction. , 1990, Brain : a journal of neurology.

[28]  L. Henderson,et al.  Serial reaction time learning and Parkinson's disease: Evidence for a procedural learning deficit , 1995, Neuropsychologia.

[29]  W. T. Thach,et al.  Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. , 1996, Brain : a journal of neurology.

[30]  A. Graybiel,et al.  Adaptive neural networks in the basal ganglia. , 1995 .

[31]  L. Squire,et al.  Parallel brain systems for learning with and without awareness. , 1994, Learning & memory.

[32]  Shawn W. Ell,et al.  The neurobiology of human category learning , 2001, Trends in Cognitive Sciences.

[33]  W Todd Maddox,et al.  Information-integration category learning in patients with striatal dysfunction. , 2005, Neuropsychology.

[34]  M. Hallett,et al.  International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome , 1997, Journal of the Neurological Sciences.

[35]  Gregory Ashby,et al.  A neuropsychological theory of multiple systems in category learning. , 1998, Psychological review.

[36]  M. Ullman A neurocognitive perspective on language: The declarative/procedural model , 2001, Nature Reviews Neuroscience.

[37]  K. Flowers Visual "closed-loop" and "open-loop" characteristics of voluntary movement in patients with Parkinsonism and intention tremor. , 1976, Brain : a journal of neurology.

[38]  Keinosuke Fukunaga,et al.  Introduction to Statistical Pattern Recognition , 1972 .

[39]  J. Kruschke,et al.  Rules and exemplars in category learning. , 1998, Journal of experimental psychology. General.

[40]  Edward E. Smith,et al.  Alternative strategies of categorization , 1998, Cognition.

[41]  S. Fahn Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale , 1987 .

[42]  Gregory Ashby,et al.  Decision rules in the perception and categorization of multidimensional stimuli. , 1988, Journal of experimental psychology. Learning, memory, and cognition.

[43]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[44]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  W. T. Thach,et al.  Throwing while looking through prisms , 2005 .

[46]  J. C. Fentress,et al.  Natural syntax rules control action sequence of rats , 1987, Behavioural Brain Research.

[47]  M. Gluck,et al.  Dissociating Hippocampal versus Basal Ganglia Contributions to Learning and Transfer , 2003, Journal of Cognitive Neuroscience.

[48]  Edward E. Smith,et al.  Categories and concepts , 1984 .

[49]  William K. Estes,et al.  Classification and cognition , 1994 .

[50]  Alan M. Wing,et al.  A comparison of the rate of pinch grip force increases and decreases in Parkinsonian bradykinesia , 1988, Neuropsychologia.

[51]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[52]  B. Rockstroh,et al.  The cerebellum contributes to mental skills. , 1989 .

[53]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[54]  C. Marsden,et al.  Internal versus external cues and the control of attention in Parkinson's disease. , 1988, Brain : a journal of neurology.

[55]  S. Keele,et al.  Toward a Functional Analysis of the Basal Ganglia , 1998, Journal of Cognitive Neuroscience.

[56]  C. Marsden,et al.  Learning manual pursuit tracking skills in patients with Parkinson's disease. , 1997, Brain : a journal of neurology.

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

[58]  Shawn W. Ell,et al.  Category learning deficits in Parkinson's disease. , 2003, Neuropsychology.

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

[60]  F. Gregory Ashby,et al.  Multidimensional models of categorization. , 1992 .

[61]  L. Squire "Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans": Correction. , 1992 .

[62]  N. Perrin,et al.  Varieties of perceptual independence. , 1986, Psychological review.

[63]  G. Goldberg Supplementary motor area structure and function: Review and hypotheses , 1985, Behavioral and Brain Sciences.

[64]  R. Shadmehr,et al.  Motor disorder in Huntington's disease begins as a dysfunction in error feedback control , 2000, Nature.

[65]  W. Meck Functional and neural mechanisms of interval timing , 2003 .

[66]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[67]  M. Gluck,et al.  Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. , 2004, Brain : a journal of neurology.

[68]  S. Kéri The cognitive neuroscience of category learning , 2003, Brain Research Reviews.

[69]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[70]  B. Djahanguiri,et al.  The prevention of acute gastric ulcer in the rat by alpha-methyldopa. , 1967, Medicina et pharmacologia experimentalis. International journal of experimental medicine.

[71]  W T Maddox,et al.  Comparing decision bound and exemplar models of categorization , 1993, Perception & psychophysics.

[72]  Richard B. Ivry,et al.  Comparison of the Basal Ganglia and Cerebellum in Shifting Attention. , 2001, Journal of Cognitive Neuroscience.

[73]  A. Bonnet [The Unified Parkinson's Disease Rating Scale]. , 2000, Revue neurologique.

[74]  Karl J. Friston,et al.  Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[76]  J. Desmond,et al.  Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI , 1997, The Journal of Neuroscience.

[77]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[78]  D. Schacter Implicit memory: History and current status. , 1987 .

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

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

[81]  Irene Daum,et al.  Sequence learning in Parkinson’s disease: a comparison of spatial-attention and number-response sequences , 2000, Neuropsychologia.

[82]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[83]  F. Ashby,et al.  The effects of concurrent task interference on category learning: Evidence for multiple category learning systems , 2001, Psychonomic bulletin & review.