Neural correlates of skill acquisition: Decreased cortical activity during a serial interception sequence learning task

Learning of complex motor skills requires learning of component movements as well as the sequential structure of their order and timing. Using a Serial Interception Sequence Learning (SISL) task, participants learned a sequence of precisely timed interception responses through training with a repeating sequence. Following initial implicit learning of the repeating sequence, functional MRI data were collected during performance of that known sequence and compared with activity evoked during novel sequences of actions, novel timing patterns, or both. Reduced activity was observed during the practiced sequence in a distributed bilateral network including extrastriate occipital, parietal, and premotor cortical regions. These reductions in evoked activity likely reflect improved efficiency in visuospatial processing, spatio-motor integration, motor planning, and motor execution for the trained sequence, which is likely supported by nondeclarative skill learning. In addition, the practiced sequence evoked increased activity in the left ventral striatum and medial prefrontal cortex, while the posterior cingulate was more active during periods of better performance. Many prior studies of perceptual-motor skill learning have found increased activity in motor areas of the frontal cortex (e.g., motor and premotor cortex, SMA) and striatal areas (e.g., the putamen). The change in activity observed here (i.e., decreased activity across a cortical network) may reflect skill learning that is predominantly expressed through more accurate performance rather than decreased reaction time.

[1]  B. Hatfield,et al.  Cerebral cortical adaptations associated with visuomotor practice. , 2004, Medicine and science in sports and exercise.

[2]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[3]  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.

[4]  Francesco Lacquaniti,et al.  Contributions of the Human Temporoparietal Junction and MT/V5+ to the Timing of Interception Revealed by Transcranial Magnetic Stimulation , 2008, The Journal of Neuroscience.

[5]  M. Hallett,et al.  Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. , 2008, Cerebral cortex.

[6]  J. Ashe,et al.  Neural correlates of encoding and expression in implicit sequence learning , 2005, Experimental Brain Research.

[7]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[8]  Hyuk Oh,et al.  Cerebral cortical dynamics during visuomotor transformation: adaptation to a cognitive-motor executive challenge. , 2011, Psychophysiology.

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

[10]  C. Carter,et al.  Regional brain activation during concurrent implicit and explicit sequence learning. , 2004, Cerebral cortex.

[11]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

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

[13]  S. Rauch,et al.  Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging , 1997, Human brain mapping.

[14]  E. Robertson The Serial Reaction Time Task: Implicit Motor Skill Learning? , 2007, The Journal of Neuroscience.

[15]  Andreas A Ioannides,et al.  Stimulus‐contrast‐induced biases in activation order reveal interaction between V1/V2 and human MT+ , 2009, Human brain mapping.

[16]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[17]  Tsung-Min Hung,et al.  Electroencephalographic Studies of Skilled Psychomotor Performance , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[18]  Jing Z. Liu,et al.  Relationship between muscle output and functional MRI-measured brain activation , 2001, Experimental Brain Research.

[19]  C D Frith,et al.  On the benefits of not trying: brain activity and connectivity reflecting the interactions of explicit and implicit sequence learning. , 2005, Cerebral cortex.

[20]  Daniel J. Sanchez,et al.  Performing the unexplainable: Implicit task performance reveals individually reliable sequence learning without explicit knowledge , 2010, Psychonomic bulletin & review.

[21]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement extent and speed. , 2003, Journal of neurophysiology.

[22]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[23]  Paul J. Reber,et al.  Dissociating Explicit and Implicit Category Knowledge with fMRI , 2003, Journal of Cognitive Neuroscience.

[24]  Katsuyuki Sakai,et al.  Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. , 2002, Journal of neurophysiology.

[25]  J. Gabrieli,et al.  Direct comparison of neural systems mediating conscious and unconscious skill learning. , 2002, Journal of neurophysiology.

[26]  Tao Liu,et al.  Differential Effect of Reward and Punishment on Procedural Learning , 2009, The Journal of Neuroscience.

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

[28]  Paul J Reber,et al.  Priming effects in the fusiform gyrus: changes in neural activity beyond the second presentation. , 2005, Cerebral cortex.

[29]  W. Schultz,et al.  Neuronal activity in monkey ventral striatum related to the expectation of reward , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[31]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[32]  K. A. Ericsson,et al.  Science Current Directions in Psychological of Expert and Exceptional Performance Capturing the Naturally Occurring Superior Performance of Experts in the Laboratory : toward a Science on Behalf Of: Association for Psychological Science , 2022 .

[33]  M. Desseilles,et al.  Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory , 2008, Neuron.

[34]  Jill X O'Reilly,et al.  Acquisition of the temporal and ordinal structure of movement sequences in incidental learning. , 2008, Journal of neurophysiology.

[35]  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.

[36]  C. Carter,et al.  Complementary Category Learning Systems Identified Using Event-Related Functional MRI , 2000, Journal of Cognitive Neuroscience.

[37]  Paul J Reber,et al.  Integration of temporal and ordinal information during serial interception sequence learning. , 2011, Journal of experimental psychology. Learning, memory, and cognition.

[38]  M. Csíkszentmihályi Flow. The Psychology of Optimal Experience. New York (HarperPerennial) 1990. , 1990 .

[39]  E. Koechlin,et al.  Serial Organization of Human Behavior in the Inferior Parietal Cortex , 2007, The Journal of Neuroscience.

[40]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[41]  Claudio Del Percio,et al.  “Neural efficiency” of athletes’ brain for upright standing: A high-resolution EEG study , 2009, Brain Research Bulletin.

[42]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  Axel Cleeremans,et al.  Striatum forever, despite sequence learning variability: A random effect analysis of PET data , 2000, Human brain mapping.

[44]  Michael A Yassa,et al.  A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe , 2009, NeuroImage.

[45]  G. Berns,et al.  Brain regions responsive to novelty in the absence of awareness. , 1997, Science.

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

[47]  M. Weatherall,et al.  Is implicit sequence learning impaired in Parkinson's disease? A meta-analysis. , 2006, Neuropsychology.

[48]  Richard B Ivry,et al.  Concurrent learning of temporal and spatial sequences. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[49]  Julien Doyon,et al.  The multifaceted nature of the relationship between performance and brain activity in motor sequence learning , 2010, NeuroImage.

[50]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

[51]  D. Schacter,et al.  Reductions in cortical activity during priming , 2007, Current Opinion in Neurobiology.

[52]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[53]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.