Distinct striatal regions for planning and executing novel and automated movement sequences

The basal ganglia-thalamo-cortical circuits are viewed as segregated parallel feed back loops crucially involved in motor control, cognition, and emotional processing. Their role in planning novel, as compared to overlearned movement patterns is as yet not well defined. We tested for the involvement of the associative striatum (caudate/anterior putamen) in the generation of novel movement patterns, which is a critical cognitive requirement for non-routine motor behavior. Using event related functional MRI in 14 right-handed male subjects, we analyzed brain activity in the planning phase of four digit finger sequences. Subjects either executed a single overlearned four digit sequence (RECALL), or self-determined four digit sequences of varying order (GENERATE). In both conditions, RECALL and GENERATE, planning was associated with activation in mesial/lateral premotor cortices, motor cingulate cortex, superior parietal cortex, basal ganglia, insula, thalamus, and midbrain nuclei. When contrasting the planning phase of GENERATE with the planning phase of RECALL, there was significantly higher activation within this distributed network. At the level of the basal ganglia, the planning phase of GENERATE was associated with differentially higher activation located specifically within the associative striatum bilaterally. On the other hand, the execution phase during both conditions was associated with a shift of activity towards the posterior part of the putamen. Our data show the specific involvement of the associative striatum during the planning of non-routine movement patterns and illustrate the propagation of activity from rostral to dorsal basal ganglia sites during different stages of motor processing.

[1]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  P. Matthews,et al.  Changing brain networks for visuomotor control with increased movement automaticity. , 2004, Journal of neurophysiology.

[3]  K. Nakano,et al.  Neural circuits and functional organization of the striatum , 2000, Journal of Neurology.

[4]  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.

[5]  Mario F. Mendez,et al.  Neurobehavioral changes associated with caudate lesions , 1989, Neurology.

[6]  A. Afifi,et al.  The basal ganglia: a neural network with more than motor function. , 2003, Seminars in pediatric neurology.

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

[8]  A. Dagher,et al.  Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. , 2006, Cerebral cortex.

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

[10]  G. E. Alexander,et al.  Functional organization of the basal ganglia: contributions of single-cell recording studies. , 1984, Ciba Foundation symposium.

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

[12]  Kenji Doya,et al.  fMRI investigation of cortical and subcortical networks in the learning of abstract and effector-specific representations of motor sequences , 2006, NeuroImage.

[13]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[14]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. Pandya,et al.  Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys , 1991, The Journal of comparative neurology.

[16]  M. Piccirilli,et al.  Frontal lobe dysfunction in Parkinson's disease: prognostic value for dementia? , 1989, European neurology.

[17]  Paul M. Grasby,et al.  A positron emission tomography (PET) investigation of the role of striatal dopamine (D2) receptor availability in spatial cognition , 2005, NeuroImage.

[18]  Takashi Hanakawa,et al.  The representation of blinking movement in cingulate motor areas: a functional magnetic resonance imaging study. , 2008, Cerebral cortex.

[19]  G Winocur,et al.  Prefrontal cortex and caudate nucleus in conditional associative learning: dissociated effects of selective brain lesions in rats. , 1998, Behavioral neuroscience.

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

[21]  P. Goldman-Rakic,et al.  Differential Activation of the Caudate Nucleus in Primates Performing Spatial and Nonspatial Working Memory Tasks , 1997, The Journal of Neuroscience.

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

[23]  Morris Moscovitch,et al.  Cognitive and motor functioning in a patient with selective infarction of the left basal ganglia: evidence for decreased non-routine response selection and performance , 2004, Neuropsychologia.

[24]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[25]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[26]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[27]  H. Künzle.  Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[28]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[29]  Deborah L. Harrington,et al.  From preparation to online control: Reappraisal of neural circuitry mediating internally generated and externally guided actions , 2006, NeuroImage.

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

[31]  Alan C. Evans,et al.  Planning and Spatial Working Memory: a Positron Emission Tomography Study in Humans , 1996, The European journal of neuroscience.

[32]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

[33]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.

[34]  Rainer Goebel,et al.  Independent component model of the default-mode brain function: Assessing the impact of active thinking , 2006, Brain Research Bulletin.

[35]  Kenneth F. Valyear,et al.  Dissociating Arbitrary Stimulus-Response Mapping from Movement Planning during Preparatory Period: Evidence from Event-Related Functional Magnetic Resonance Imaging , 2006, The Journal of Neuroscience.

[36]  Mark Hallett,et al.  CASL fMRI of subcortico-cortical perfusion changes during memory-guided finger sequences , 2005, NeuroImage.

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

[38]  Ewald Moser,et al.  The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response , 2003, NeuroImage.

[39]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

[40]  A. Nambu,et al.  Organization of corticostriatal motor inputs in monkey putamen. , 2002, Journal of neurophysiology.

[41]  Heidi Johansen-Berg,et al.  Model-free characterization of brain functional networks for motor sequence learning using fMRI , 2008, NeuroImage.

[42]  M. H Beauchamp,et al.  Dynamic functional changes associated with cognitive skill learning of an adapted version of the Tower of London task , 2003, NeuroImage.

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

[44]  M. Petrides,et al.  Cortical activity in Parkinson's disease during executive processing depends on striatal involvement. , 2006, Brain : a journal of neurology.

[45]  M. Hallett,et al.  Frontal and parietal networks for conditional motor learning: a positron emission tomography study. , 1997, Journal of neurophysiology.

[46]  M. Inase,et al.  Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: comparison with the input zones from the supplementary motor area , 1999, Brain Research.

[47]  G. Figiel,et al.  Neurobehavioral changes with caudate lesions , 1989, Neurology.

[48]  J. Jankowski,et al.  A role of the basal ganglia and midbrain nuclei for initiation of motor sequences , 2008, NeuroImage.

[49]  R. Ridley,et al.  Sensorimotor deficits in a unilateral intrastriatal 6-OHDA partial lesion model of Parkinson’s disease in marmoset monkeys , 2003, Experimental Neurology.

[50]  M. Petrides,et al.  Functional role of the basal ganglia in the planning and execution of actions , 2006, Annals of neurology.

[51]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[52]  Jean-Baptiste Poline,et al.  Distinct striatal regions support movement selection, preparation and execution , 2004, Neuroreport.

[53]  J. Hollerman,et al.  Influence of reward expectation on behavior-related neuronal activity in primate striatum. , 1998, Journal of neurophysiology.

[54]  G. Heit,et al.  Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels , 2005, Brain Research Reviews.

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

[56]  Karl J. Friston,et al.  Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. , 1998, Journal of neurophysiology.

[57]  Xiaofeng Lu,et al.  Somatotopically arranged inputs from putamen and subthalamic nucleus to primary motor cortex , 2006, Neuroscience Research.

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

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

[60]  D Bonner,et al.  Acute Frontal Lobe Syndrome and Dyscontrol Associated with Bilateral Caudate Nucleus Infarctions , 1996, British Journal of Psychiatry.

[61]  J. Saint-Cyr,et al.  Frontal lobe dysfunction in Parkinson's disease. The cortical focus of neostriatal outflow. , 1986, Brain : a journal of neurology.

[62]  Ewald Moser,et al.  Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. , 2005, Human movement science.

[63]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[64]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[65]  Paul E. Gilbert,et al.  The role of the medial caudate nucleus, but not the hippocampus, in a matching‐to sample task for a motor response , 2006, The European journal of neuroscience.

[66]  B Conrad,et al.  Time-resolved fMRI of activation patterns in M1 and SMA during complex voluntary movement. , 2001, Journal of neurophysiology.

[67]  Henk J Groenewegen,et al.  Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. , 2005, Archives of general psychiatry.

[68]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[69]  Chantal E. Stern,et al.  An fMRI investigation of the role of the basal ganglia in reasoning , 2007, Brain Research.

[70]  Frederik Barkhof,et al.  Frontostriatal system in planning complexity: a parametric functional magnetic resonance version of tower of london task , 2003, NeuroImage.

[71]  A. Dagher,et al.  The role of the striatum and hippocampus in planning: a PET activation study in Parkinson's disease. , 2001, Brain : a journal of neurology.

[72]  M. Inase,et al.  Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex , 1998, Experimental Brain Research.

[73]  A. Dagher,et al.  Mapping the network for planning: a correlational PET activation study with the Tower of London task. , 1999, Brain : a journal of neurology.