3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum.

Studies in non-human primates have shown that medial premotor projections to the striatum are characterized as a set of distinct circuits conveying different type of information. This study assesses the anatomical projections from the supplementary motor area (SMA), pre-SMA and motor cortex (MC) to the human striatum using diffusion tensor imaging (DTI) axonal tracking. Eight right-handed volunteers were studied at 1.5 T using DTI axonal tracking. A connectivity matrix was computed, which tested for connections between cortical areas (MC, SMA and pre-SMA) and subcortical areas (posterior, middle and anterior putamen and the head of the caudate nucleus) in each hemisphere. Pre-SMA projections to the striatum were located rostral to SMA projections to the striatum. The SMA and the MC were similarly connected to the posterior and middle putamen and not to the anterior striatum. These data show that the MC and SMA have connections with similar parts of the sensorimotor compartment of the human striatum, whereas the pre-SMA sends connections to more rostral parts of the striatum, including the associative compartment.

[1]  R. Ursin Sleep stage relations within the sleep cycles of the cat. , 1970, Brain research.

[2]  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.

[3]  H. Künzle An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. , 1978, Brain, behavior and evolution.

[4]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[6]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[7]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[8]  P. Goldman-Rakic,et al.  Interhemispheric integration: I. Symmetry and convergence of the corticocortical connections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) in the rhesus monkey. , 1991, Cerebral cortex.

[9]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[10]  P. Goldman-Rakic,et al.  Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. , 1991, Cerebral cortex.

[11]  A. Graybiel,et al.  Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. , 1991, Journal of neurophysiology.

[12]  A. Graybiel,et al.  Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  J. Binder,et al.  Functional magnetic resonance imaging of complex human movements , 1993, Neurology.

[14]  A. Graybiel,et al.  Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[16]  L. Hazrati,et al.  Functional anatomy of the basal ganglia , 1995 .

[17]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

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

[19]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[20]  Jun Tanji,et al.  New concepts of the supplementary motor area , 1996, Current Opinion in Neurobiology.

[21]  M Wiesendanger,et al.  Is the supplementary motor area a bilaterally organized system? , 1996, Advances in neurology.

[22]  G Rizzolatti,et al.  The classic supplementary motor area is formed by two independent areas. , 1996, Advances in neurology.

[23]  Guy Marchal,et al.  Multi-modality image registration by maximization of mutual information , 1996, Proceedings of the Workshop on Mathematical Methods in Biomedical Image Analysis.

[24]  J Tanji,et al.  Overlapping corticostriatal projections from the supplementary motor area and the primary motor cortex in the macaque monkey: An anterograde double labeling study , 1996, The Journal of comparative neurology.

[25]  James R. Moore,et al.  Correction for distortion of echo‐planar images used to calculate the apparent diffusion coefficient , 1996, Magnetic resonance in medicine.

[26]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[27]  S Clare,et al.  Functional magnetic resonance imaging of single motor events reveals human presupplementary motor area , 1997, Annals of neurology.

[28]  Masahiko Inase,et al.  Corticostriatal input zones from the supplementary motor area overlap those from the contra- rather than ipsilateral primary motor cortex , 1998, Brain Research.

[29]  O. Hikosaka,et al.  Presupplementary Motor Area Activation during Sequence Learning Reflects Visuo-Motor Association , 1999, The Journal of Neuroscience.

[30]  K Friston,et al.  Signal-, set- and movement-related activity in the human brain: an event-related fMRI study. , 1999, Cerebral cortex.

[31]  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.

[32]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[33]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[35]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[36]  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.

[37]  C. Poupon,et al.  Regularization of Diffusion-Based Direction Maps for the Tracking of Brain White Matter Fascicles , 2000, NeuroImage.

[38]  D. Le Bihan,et al.  Role of the supplementary motor area in motor deficit following medial frontal lobe surgery , 2001, Neurology.

[39]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[40]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[41]  Isabelle Bloch,et al.  Distortion correction and robust tensor estimation for MR diffusion imaging , 2002, Medical Image Anal..

[42]  Stéphane Lehéricy,et al.  Normal functional imaging of the basal ganglia. , 2002, Epileptic disorders : international epilepsy journal with videotape.

[43]  Thierry Wannier,et al.  Origins of callosal projections to the supplementary motor area (SMA): A direct comparison between pre‐SMA and SMA‐proper in macaque monkeys , 2002, The Journal of comparative neurology.

[44]  W. Schultz,et al.  Role of primate basal ganglia and frontal cortex in the internal generation of movements , 2004, Experimental Brain Research.

[45]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[46]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.