Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study.

We examined the dynamic involvement of different brain regions in implicit and explicit motor sequence learning using PET. In a serial reaction time task, subjects pressed each of four buttons with a different finger of the right hand in response to a visually presented number. Test sessions consisted of 10 cycles of the same 10-item sequence. The effects of explicit and implicit learning were assessed separately using a different behavioural parameter for each type of learning: correct recall of the test sequence for explicit learning and improvement of reaction time before the successful recall of any component of the test sequence for implicit learning. Regional cerebral blood flow was measured repeatedly during the task, and a parametric analysis was performed to identify brain regions in which activity was significantly correlated with subjects' performances: i.e. with correct recall of the test sequence or with reaction time. Explicit learning, shown as a positive correlation with the correct recall of the sequence, was associated with increased activity in the posterior parietal cortex, precuneus and premotor cortex bilaterally, also in the supplementary motor area (SMA) predominantly in the left anterior part, left thalamus, and right dorsolateral prefrontal cortex. In contrast, the reaction time showed a different pattern of correlation during different learning phases. During the implicit learning phase, when the subjects were not aware of the sequence, improvement of the reaction time was associated with increased activity in the contralateral primary sensorimotor cortex (SM1). During the explicit learning phase, the reaction time was significantly correlated with activity in a part of the frontoparietal network. During the post-learning phase, when the subjects achieved all components of the sequence explicitly, the reaction time was correlated with the activity in the ipsilateral SM1 and posterior part of the SMA. These results show that different sets of cortical regions are dynamically involved in implicit and explicit motor sequence learning.

[1]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

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

[3]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[4]  A. Luria Higher Cortical Functions in Man , 1980, Springer US.

[5]  M. Mintun,et al.  A Noninvasive Approach to Quantitative Functional Brain Mapping with H215O and Positron Emission Tomography , 1984, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  M. Raichle,et al.  Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. , 1984, Journal of neurophysiology.

[7]  D. Schacter,et al.  Implicit and explicit memory for new associations in normal and amnesic subjects. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[8]  L. Squire Memory and Brain , 1987 .

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

[10]  Takashi Sakamoto,et al.  Long-lasting potentiation of synaptic potentials in the motor cortex produced by stimulation of the sensory cortex in the cat: a basis of motor learning , 1987, Brain Research.

[11]  M. Nissen,et al.  Implicit learning in patients with probable Alzheimer's disease , 1987, Neurology.

[12]  J. Saint-Cyr,et al.  Procedural learning and neostriatal dysfunction in man. , 1988, Brain : a journal of neurology.

[13]  M. Mintun,et al.  Noninvasive functional brain mapping by change-distribution analysis of averaged PET images of H215O tissue activity. , 1989, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[14]  Peter Bullemer,et al.  On the development of procedural knowledge. , 1989 .

[15]  H. Asanuma,et al.  Functional role of the sensory cortex in learning motor skills in cats , 1989, Brain Research.

[16]  A. Keller,et al.  Long-term potentiation in the motor cortex. , 1989, Science.

[17]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[18]  Richard I. Ivry,et al.  Attention and structure in sequence learning. , 1990 .

[19]  H. Freund,et al.  Premotor cortex and conditional motor learning in man. , 1990, Brain : a journal of neurology.

[20]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[21]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  M. Petrides Functional specialization within the dorsolateral frontal cortex for serial order memory , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  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.

[24]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  D L Schacter,et al.  Implicit knowledge: new perspectives on unconscious processes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Karl J. Friston,et al.  Regional response differences within the human auditory cortex when listening to words , 1992, Neuroscience Letters.

[27]  M. Amorim,et al.  Conscious knowledge and changes in performance in sequence learning: evidence against dissociation. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[28]  Á. Pascual-Leone,et al.  Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. , 1993, Brain : a journal of neurology.

[29]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[30]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  D. Schacter,et al.  Implicit memory: a selective review. , 1993, Annual review of neuroscience.

[32]  H Shibasaki,et al.  Enhanced negative slope of cortical potentials before sequential as compared with simultaneous extensions of two fingers. , 1993, Electroencephalography and clinical neurophysiology.

[33]  R. Passingham The frontal lobes and voluntary action , 1993 .

[34]  Tim Curran,et al.  Attentional and Nonattentional Forms of Sequence Learning , 1993 .

[35]  H. Asanuma,et al.  Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. , 1993, Journal of neurophysiology.

[36]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[37]  Scott T. Grafton,et al.  Functional imaging of procedural motor learning: Relating cerebral blood flow with individual subject performance , 1994, Human brain mapping.

[38]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

[40]  P. Frensch,et al.  Effects of presentation rate and individual differences in short-term memory capacity on an indirect measure of serial learning , 1994, Memory & cognition.

[41]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[42]  S. Kosslyn,et al.  A PET investigation of implicit and explicit sequence learning , 1995 .

[43]  J. Saint-Cyr,et al.  Behavior and the basal ganglia. , 1995, Advances in neurology.

[44]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[45]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[46]  David A. Caulton,et al.  On the Modularity of Sequence Representation , 1995 .

[47]  J C Mazziotta,et al.  Effects of stimulus rate on regional cerebral blood flow after median nerve stimulation. , 1995, Brain : a journal of neurology.

[48]  S. Wise,et al.  Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. , 1995, Journal of neurophysiology.

[49]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[50]  D. Brooks The role of the basal ganglia in motor control: contributions from PET , 1995, Journal of the Neurological Sciences.

[51]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[52]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[53]  A. Berthoz,et al.  Functional Anatomy of a Prelearned Sequence of Horizontal Saccades in Humans , 1996, The Journal of Neuroscience.

[54]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  M. Hallett,et al.  Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[56]  Alan C. Evans,et al.  Functional Anatomy of Visuomotor Skill Learning in Human Subjects Examined with Positron Emission Tomography , 1996, The European journal of neuroscience.

[57]  S. Kiebel,et al.  Brain Representation of Active and Passive Movements , 1996, NeuroImage.

[58]  O. Hikosaka,et al.  Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. , 1996, Journal of neurophysiology.

[59]  M Hallett,et al.  Event-related desynchronization (ERD) in the alpha frequency during development of implicit and explicit learning. , 1997, Electroencephalography and clinical neurophysiology.

[60]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. II. Subcortical structures and learning by trial and error. , 1997, Journal of neurophysiology.

[61]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[62]  S Kornblum,et al.  Dynamics of Single Neuron Activity in Monkey Primary Motor Cortex Related to Sensorimotor Transformation , 1997, The Journal of Neuroscience.

[63]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[64]  Herbert Heuer,et al.  Task integration as a factor in secondary-task effects on sequence learning , 1997 .

[65]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.