A Neurocomputational Model of Automatic Sequence Production

Most behaviors unfold in time and include a sequence of submovements or cognitive activities. In addition, most behaviors are automatic and repeated daily throughout life. Yet, relatively little is known about the neurobiology of automatic sequence production. Past research suggests a gradual transfer from the associative striatum to the sensorimotor striatum, but a number of more recent studies challenge this role of the BG in automatic sequence production. In this article, we propose a new neurocomputational model of automatic sequence production in which the main role of the BG is to train cortical–cortical connections within the premotor areas that are responsible for automatic sequence production. The new model is used to simulate four different data sets from human and nonhuman animals, including (1) behavioral data (e.g., RTs), (2) electrophysiology data (e.g., single-neuron recordings), (3) macrostructure data (e.g., TMS), and (4) neurological circuit data (e.g., inactivation studies). We conclude with a comparison of the new model with existing models of automatic sequence production and discuss a possible new role for the BG in automaticity and its implication for Parkinson's disease.

[1]  Benjamin A Clegg,et al.  Sequence learning , 1998, Trends in Cognitive Sciences.

[2]  J. Tanji,et al.  Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. , 2000, Journal of neurophysiology.

[3]  J. Houk,et al.  Cerebellar guidance of premotor network development and sensorimotor learning. , 1997, Learning & memory.

[4]  P. Strick,et al.  New concepts about the organization of basal ganglia output. , 1997, Advances in neurology.

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

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

[7]  Sébastien Hélie,et al.  A neurocomputational account of cognitive deficits in Parkinson's disease , 2012, Neuropsychologia.

[8]  P. Strick,et al.  An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. , 2003, Journal of neurophysiology.

[9]  Joel L. Davis,et al.  Macro-organization of the Circuits Connecting the Basal Ganglia with the Cortical Motor Areas , 1994 .

[10]  Jack van Honk,et al.  On the role of the SMA in the discrete sequence production task: a TMS study , 2002, Neuropsychologia.

[11]  Gillian M Clark,et al.  A meta-analysis and meta-regression of serial reaction time task performance in Parkinson's disease. , 2014, Neuropsychology.

[12]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[13]  R. Sun,et al.  The interaction of the explicit and the implicit in skill learning: a dual-process approach. , 2005, Psychological review.

[14]  F. Gregory Ashby,et al.  Evidence for Cortical Automaticity in Rule-Based Categorization , 2010, The Journal of Neuroscience.

[15]  Shawn W. Ell,et al.  Learning robust cortico-cortical associations with the basal ganglia: An integrative review , 2015, Cortex.

[16]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[17]  Michel Desmurget,et al.  Motor Sequences and the Basal Ganglia: Kinematics, Not Habits , 2010, The Journal of Neuroscience.

[18]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[19]  M. Feenstra,et al.  Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling and exposure to novelty , 1996, Brain Research.

[20]  Axel Cleeremans,et al.  Computational Models of Implicit Learning , 2019, Implicit Learning.

[21]  A. Heathcote,et al.  Averaging learning curves across and within participants , 2003, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[22]  John C. Rothwell,et al.  The theoretical model of theta burst form of repetitive transcranial magnetic stimulation , 2011, Clinical Neurophysiology.

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

[24]  Axel Cleeremans,et al.  Attention and awareness in sequence learning , 1993 .

[25]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[26]  K. Doya,et al.  Parallel Cortico-Basal Ganglia Mechanisms for Acquisition and Execution of Visuomotor SequencesA Computational Approach , 2001, Journal of Cognitive Neuroscience.

[27]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[28]  Sébastien Hélie,et al.  Bottom-up learning of explicit knowledge using a Bayesian algorithm and a new Hebbian learning rule , 2011, Neural Networks.

[29]  A. Flaherty,et al.  Input-output organization of the sensorimotor striatum in the squirrel monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Benjamin O. Turner,et al.  Cortical and basal ganglia contributions to habit learning and automaticity , 2010, Trends in Cognitive Sciences.

[31]  Charles R. Gerfen,et al.  The Neuroanatomical Organization of the Basal Ganglia , 2010 .

[32]  P. Strick,et al.  Skill representation in the primary motor cortex after long-term practice. , 2007, Journal of neurophysiology.

[33]  Jonathan D. Wallis,et al.  A Comparison of Abstract Rules in the Prefrontal Cortex, Premotor Cortex, Inferior Temporal Cortex, and Striatum , 2006, Journal of Cognitive Neuroscience.

[34]  John M. Ennis,et al.  A neurobiological theory of automaticity in perceptual categorization. , 2007, Psychological review.

[35]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[36]  L. Squire Memory systems of the brain: A brief history and current perspective , 2004, Neurobiology of Learning and Memory.

[37]  W. Weiner,et al.  KICK AND RUSH: PARADOXICAL KINESIA IN PARKINSON DISEASE , 2009, Neurology.

[38]  Ron Sun,et al.  The Cambridge Handbook of Computational Psychology , 2008 .

[39]  Jeffrey L. Elman,et al.  Finding Structure in Time , 1990, Cogn. Sci..

[40]  O. Hikosaka,et al.  Differential activation of monkey striatal neurons in the early and late stages of procedural learning , 2002, Experimental Brain Research.

[41]  Eugene M. Izhikevich,et al.  Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting , 2006 .