Apraxia Impairs Intentional Retrieval of Incidentally Acquired Motor Knowledge

Apraxia caused by left hemispheric stroke typically impairs skilled sequential movements. After stroke, apraxic patients need to reacquire motor skills by motor learning. The current study assessed for the first time incidental motor sequence learning in apraxic patients. Forty-eight human subjects (henceforth called “patients”) with left hemispheric stroke affecting the middle cerebral artery territory (18 with apraxia and 30 without apraxia) and 17 age-matched healthy controls were tested on a visuomanual serial reaction time task. Subjects performed four blocks consisting of repetitions of a complex six element sequence containing ambiguous pairwise transitions before a new and unfamiliar sequence was introduced in block 5. Reaction time (RT) disadvantages in this fifth block indicated incidental sequence-specific motor learning. The intentional retrieval of the learned motor knowledge was assessed subsequently with a free recall task. Voxel-based lesion-symptom mapping (VLSM) was performed to investigate for the first time the lesion correlates of deficits in learning and retrieving sequential motor knowledge. Despite generally prolonged RTs, apraxic patients showed sequence-specific motor learning as could be observed in nonapraxic patients and healthy controls. However, apraxic patients showed reduced intentional retrieval of the learned sequence. VLSM revealed that impaired intentional retrieval of motor sequence knowledge resulted from dorsal premotor cortex lesions. Apraxic patients showed a dissociation of preserved incidental motor (sequence) learning and deficient intentional retrieval of this incidentally learned motor knowledge. The data suggest that novel approaches for treating apraxia should focus on incidental motor learning, but that automatic rather than intentional retrieval strategies should be enforced.

[1]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C D Marsden,et al.  Limb apraxias: higher-order disorders of sensorimotor integration. , 2000, Brain : a journal of neurology.

[3]  K. Heilman,et al.  Acquisition and retention of gestures by apraxic patients , 1984, Brain and Cognition.

[4]  Anne Springer,et al.  Predicting and memorizing observed action: Differential premotor cortex involvement , 2011, Human brain mapping.

[5]  J. Hermsdörfer,et al.  Cortical Correlates of Gesture Processing: Clues to the Cerebral Mechanisms Underlying Apraxia during the Imitation of Meaningless Gestures , 2001, NeuroImage.

[6]  J. Hermsdörfer,et al.  Neural representations of pantomimed and actual tool use: Evidence from an event-related fMRI study , 2007, NeuroImage.

[7]  R. Lyle A performance test for assessment of upper limb function in physical rehabilitation treatment and research , 1981, International journal of rehabilitation research. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation.

[8]  K. Lovblad,et al.  Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. , 2010, Brain : a journal of neurology.

[9]  G. Goldenberg Defective imitation of gestures in patients with damage in the left or right hemispheres. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[10]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[11]  Georg Goldenberg,et al.  The Neural Basis of Imitation is Body Part Specific , 2006, The Journal of Neuroscience.

[12]  Peder J. Johnson,et al.  Assessing implicit learning with indirect tests: Determining what is learned about sequence structure. , 1994 .

[13]  P. Weiss,et al.  [How to diagnose and treat limb apraxia]. , 2011, Fortschritte der Neurologie-Psychiatrie.

[14]  J. Rankin Cerebral Vascular Accidents in Patients over the Age of 60: II. Prognosis , 1957, Scottish medical journal.

[15]  J. Hermsdörfer,et al.  It takes the whole brain to make a cup of coffee: the neuropsychology of naturalistic actions involving technical devices , 2005, Neuropsychologia.

[16]  Yong Li,et al.  Different left brain regions are essential for grasping a tool compared with its subsequent use , 2010, NeuroImage.

[17]  J Hermsdörfer,et al.  The effect of tactile feedback on pantomime of tool use in apraxia , 2004, Neurology.

[18]  E. Renzi,et al.  Ideational apraxia: A quantitative study , 1968 .

[19]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[20]  E. Renzi,et al.  The token test: A sensitive test to detect receptive disturbances in aphasics. , 1962, Brain : a journal of neurology.

[21]  Z. Dienes,et al.  Implicit learning: Below the subjective threshold , 1997 .

[22]  Mark Mühlau,et al.  Left inferior parietal dominance in gesture imitation: an fMRI study , 2005, Neuropsychologia.

[23]  D. Harrington,et al.  Motor sequencing with left hemisphere damage. Are some cognitive deficits specific to limb apraxia? , 1992, Brain : a journal of neurology.

[24]  R. Masters,et al.  Implicit sequence learning processes after unilateral stroke , 2007, Neuropsychological rehabilitation.

[25]  L. Buxbaum,et al.  Ideational apraxia and naturalistic action. , 1998, Cognitive neuropsychology.

[26]  K M Heilman,et al.  Three-dimensional computergraphic analysis of apraxia. Neural representations of learned movement. , 1990, Brain : a journal of neurology.

[27]  N Motomura,et al.  Motor learning in ideomotor apraxia. , 1989, The International journal of neuroscience.

[28]  Mark Hallett,et al.  Treatment of limb apraxia: moving forward to improved action. , 2008, American journal of physical medicine & rehabilitation.

[29]  D. Filion,et al.  Implicit learning of a motor skill after mild and moderate stroke , 2006, Clinical rehabilitation.

[30]  P. Weiss,et al.  Deficient sequencing of pantomimes in apraxia , 2008, Neurology.

[31]  I. Koch,et al.  Learning hierarchically structured action sequences is unaffected by prefrontal-cortex lesion , 2006, Experimental Brain Research.

[32]  Kenichi Ohki,et al.  Conversion of Working Memory to Motor Sequence in the Monkey Premotor Cortex , 2003, Science.

[33]  M Eimer,et al.  Explicit and implicit learning of event sequences: evidence from event-related brain potentials. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[34]  R. E Passingham,et al.  Cerebral dominance for action in the human brain: the selection of actions , 2001, Neuropsychologia.

[35]  N. Geschwind,et al.  Defective motor learning in ideomotor apraxia , 1975, Neurology.

[36]  R. Passingham,et al.  Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. , 1998, Brain : a journal of neurology.

[37]  K M Heilman,et al.  Spatial planning deficits in limb apraxia. , 1994, Brain : a journal of neurology.

[38]  E. Renzi,et al.  Performance of Left Brain-Damaged Patients on Imitation of Single Movements and Motor Sequences. Frontal and Parietal-Injured Patients Compared , 1983, Cortex.

[39]  Joachim Hoffmann,et al.  Implicit learning of loosely defined structures , 1998 .

[40]  Richard I. Ivry,et al.  Attention and Structure in Sequence Learning , 2004 .

[41]  Gereon R. Fink,et al.  Neural basis of pantomiming the use of visually presented objects , 2004, NeuroImage.

[42]  F Rösler,et al.  Implicit and explicit learning of event sequences: evidence for distinct coding of perceptual and motor representations. , 2000, Acta psychologica.

[43]  S. Keele,et al.  The cognitive and neural architecture of sequence representation. , 2003, Psychological review.

[44]  Iring Koch,et al.  The impact of response mode on implicit and explicit sequence learning. , 2002, Experimental psychology.

[45]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[46]  G. Goldenberg Pantomime of object use: a challenge to cerebral localization of cognitive function , 2003, NeuroImage.

[47]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.