A Direct Cortico-Nigral Pathway as Revealed by Constrained Spherical Deconvolution Tractography in Humans

Substantia nigra is an important neuronal structure, located in the ventral midbrain, that exerts a regulatory function within the basal ganglia circuitry through the nigro-striatal pathway. Although its subcortical connections are relatively well-known in human brain, little is known about its cortical connections. The existence of a direct cortico-nigral pathway has been demonstrated in rodents and primates but only hypothesized in humans. In this study, we aimed at evaluating cortical connections of substantia nigra in vivo in human brain by using probabilistic constrained spherical deconvolution (CSD) tractography on magnetic resonance diffusion weighted imaging data. We found that substantia nigra is connected with cerebral cortex as a whole, with the most representative connections involving prefrontal cortex, precentral and postcentral gyri and superior parietal lobule. These results may be relevant for the comprehension of the pathophysiology of several neurological disorders involving substantia nigra, such as parkinson's disease, schizophrenia, and pathological addictions.

[1]  Houeto Jean-Luc.  [Parkinson's disease]. , 2022, La Revue du praticien.

[2]  Y. Smith,et al.  Substantia Nigra , 2020, Definitions.

[3]  Ruiwang Huang,et al.  Impaired topological architecture of brain structural networks in idiopathic Parkinson’s disease: a DTI study , 2017, Brain Imaging and Behavior.

[4]  A. Quartarone,et al.  Role of cortico-pallidal connectivity in the pathophysiology of dystonia. , 2016, Brain : a journal of neurology.

[5]  S. Marino,et al.  Red nucleus connectivity as revealed by constrained spherical deconvolution tractography , 2016, Neuroscience Letters.

[6]  S. Marino,et al.  Extensive Direct Subcortical Cerebellum-Basal Ganglia Connections in Human Brain as Revealed by Constrained Spherical Deconvolution Tractography , 2016, Front. Neuroanat..

[7]  D. Rujescu,et al.  The Vulnerability to Suicidal Behavior is Associated with Reduced Connectivity Strength , 2015, Front. Hum. Neurosci..

[8]  Timothy E. J. Behrens,et al.  Measuring macroscopic brain connections in vivo , 2015, Nature Neuroscience.

[9]  Gong-Jun Ji,et al.  Mapping the functional connectivity of the substantia nigra, red nucleus and dentate nucleus: A network analysis hypothesis associated with the extrapyramidal system , 2015, Neuroscience Letters.

[10]  G. Schneider,et al.  Cortico-pallidal oscillatory connectivity in patients with dystonia. , 2015, Brain : a journal of neurology.

[11]  W. Oertel,et al.  A new dopaminergic nigro-olfactory projection , 2015, Acta Neuropathologica.

[12]  S. Marino,et al.  Basal ganglia network by constrained spherical deconvolution: A possible cortico‐pallidal pathway? , 2015, Movement disorders : official journal of the Movement Disorder Society.

[13]  T. Wichmann,et al.  The cortico‐pallidal projection: An additional route for cortical regulation of the basal ganglia circuitry , 2015, Movement disorders : official journal of the Movement Disorder Society.

[14]  M. Ghilardi,et al.  Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease , 2015, Neuroradiology.

[15]  J. Grèzes,et al.  A direct amygdala‐motor pathway for emotional displays to influence action: A diffusion tensor imaging study , 2014, Human brain mapping.

[16]  Olivier Colliot,et al.  Structural connectivity differences in left and right temporal lobe epilepsy , 2014, NeuroImage.

[17]  M. Okun,et al.  Surgical Treatment of Dyskinesia in Parkinson’s Disease , 2014, Front. Neurol..

[18]  Sung Ho Jang,et al.  Differences in neural connectivity between the substantia nigra and ventral tegmental area in the human brain , 2014, Front. Hum. Neurosci..

[19]  Trygve B. Leergaard,et al.  Brain-wide map of efferent projections from rat barrel cortex , 2014, Front. Neuroinform..

[20]  S. Jang,et al.  Relationship between somatosensory function and the spinothalamocortical pathway in chronic stroke patients , 2013, Somatosensory & motor research.

[21]  Derek K. Jones,et al.  Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging , 2013, Human brain mapping.

[22]  Raymond J. Dolan,et al.  Parcellation of the human substantia nigra based on anatomical connectivity to the striatum☆ , 2013, NeuroImage.

[23]  A. Connelly,et al.  White matter fiber tractography: why we need to move beyond DTI. , 2013, Journal of neurosurgery.

[24]  L. Malkova,et al.  Topography of dyskinesias and torticollis evoked by inhibition of substantia nigra pars reticulata , 2013, Movement disorders : official journal of the Movement Disorder Society.

[25]  Alan Connelly,et al.  SIFT: Spherical-deconvolution informed filtering of tractograms , 2013, NeuroImage.

[26]  Paul L. Rosin,et al.  A pitfall in the reconstruction of fibre ODFs using spherical deconvolution of diffusion MRI data , 2013, NeuroImage.

[27]  Yang Wang,et al.  Characteristics and variability of structural networks derived from diffusion tensor imaging , 2012, NeuroImage.

[28]  Heidi Johansen-Berg,et al.  Diffusion MRI at 25: Exploring brain tissue structure and function , 2012, NeuroImage.

[29]  J. Henderson.  “Connectomic surgery”: diffusion tensor imaging (DTI) tractography as a targeting modality for surgical modulation of neural networks , 2012, Front. Integr. Neurosci..

[30]  Richard S. Frackowiak,et al.  Confirmation of functional zones within the human subthalamic nucleus: Patterns of connectivity and sub-parcellation using diffusion weighted imaging , 2012, NeuroImage.

[31]  Timothy E. J. Behrens,et al.  Human connectomics , 2012, Current Opinion in Neurobiology.

[32]  F. Zhou,et al.  Intrinsic and integrative properties of substantia nigra pars reticulata neurons , 2011, Neuroscience.

[33]  Heidi Johansen-Berg,et al.  Tractography: Where Do We Go from Here? , 2011, Brain Connect..

[34]  J. Deniau,et al.  Subthalamic nucleus high‐frequency stimulation generates a concomitant synaptic excitation–inhibition in substantia nigra pars reticulata , 2011, The Journal of physiology.

[35]  Maxime Descoteaux,et al.  Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom , 2011, NeuroImage.

[36]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

[37]  Paul M. Matthews,et al.  Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson's disease , 2010, NeuroImage.

[38]  Geoff J M Parker,et al.  Distortion correction for diffusion‐weighted MRI tractography and fMRI in the temporal lobes , 2010, Human brain mapping.

[39]  Paul Greengard,et al.  Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors , 2010, Proceedings of the National Academy of Sciences.

[40]  Mara Cercignani,et al.  Twenty‐five pitfalls in the analysis of diffusion MRI data , 2010, NMR in biomedicine.

[41]  M. Chou,et al.  Principles and Limitations of Computational Algorithms in Clinical Diffusion Tensor MR Tractography , 2010, American Journal of Neuroradiology.

[42]  R. Wise.  Roles for nigrostriatal—not just mesocorticolimbic—dopamine in reward and addiction , 2009, Trends in Neurosciences.

[43]  P. Tobler,et al.  Functional imaging of the human dopaminergic midbrain , 2009, Trends in Neurosciences.

[44]  Rachid Deriche,et al.  Deterministic and Probabilistic Tractography Based on Complex Fibre Orientation Distributions , 2009, IEEE Transactions on Medical Imaging.

[45]  Chun-Hung Yeh,et al.  Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data , 2008, NeuroImage.

[46]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[47]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[48]  Bruce Fischl,et al.  Geometrically Accurate Topology-Correction of Cortical Surfaces Using Nonseparating Loops , 2007, IEEE Transactions on Medical Imaging.

[49]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[50]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[51]  D. Hansel,et al.  Competition between Feedback Loops Underlies Normal and Pathological Dynamics in the Basal Ganglia , 2022 .

[52]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[53]  S. Haber,et al.  Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection , 2006, Neuropsychopharmacology.

[54]  Gareth J. Barker,et al.  Optimal imaging parameters for fiber-orientation estimation in diffusion MRI , 2005, NeuroImage.

[55]  Daniel C Alexander,et al.  Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[57]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

[58]  Derek K. Jones,et al.  “Squashing peanuts and smashing pumpkins”: How noise distorts diffusion‐weighted MR data , 2004, Magnetic resonance in medicine.

[59]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[60]  L. Jasmin,et al.  Rostral agranular insular cortex and pain areas of the central nervous system: A tract‐tracing study in the rat , 2004, The Journal of comparative neurology.

[61]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[62]  J. Volkmann,et al.  Introduction to the programming of deep brain stimulators , 2002, Movement disorders : official journal of the Movement Disorder Society.

[63]  H. Kita,et al.  Neostriatal and globus pallidus stimulation induced inhibitory postsynaptic potentials in entopeduncular neurons in rat brain slice preparations , 2001, Neuroscience.

[64]  T. Paus,et al.  Repetitive Transcranial Magnetic Stimulation of the Human Prefrontal Cortex Induces Dopamine Release in the Caudate Nucleus , 2001, The Journal of Neuroscience.

[65]  Anders M. Dale,et al.  A hybrid approach to the Skull Stripping problem in MRI , 2001, NeuroImage.

[66]  J. Dostrovsky,et al.  Does stimulation of the GPi control dyskinesia by activating inhibitory axons? , 2001, Movement disorders : official journal of the Movement Disorder Society.

[67]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[68]  H. Kita,et al.  Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey , 2000 .

[69]  Nikolaus R. McFarland,et al.  Convergent Inputs from Thalamic Motor Nuclei and Frontal Cortical Areas to the Dorsal Striatum in the Primate , 2000, The Journal of Neuroscience.

[70]  C. Pierpaoli,et al.  Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: Application to white matter fiber tract mapping in the human brain , 1999, Magnetic resonance in medicine.

[71]  Y. Agid,et al.  Pallidal stimulation for Parkinson's disease , 1997, Neurology.

[72]  A. Lozano,et al.  A brief history of pallidotomy. , 1997, Neurosurgery.

[73]  M. Inase,et al.  Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  P. Basser.  Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[75]  H. Kita,et al.  The cortico-nigral projection in the rat: an anterograde tracing study with biotinylated dextran amine , 1994, Brain Research.

[76]  H. Kita,et al.  The cortico-pallidal projection in the rat: an anterograde tracing study with biotinylated dextran amine , 1994, Brain Research.

[77]  M. Delong,et al.  Primate models of movement disorders of basal ganglia origin , 1990, Trends in Neurosciences.

[78]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[79]  P. Groves,et al.  Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices , 1988, Brain Research.

[80]  D. Weinberger.  Implications of normal brain development for the pathogenesis of schizophrenia. , 1987, Archives of general psychiatry.

[81]  H. Kornhuber,et al.  The cortico-nigral projection: reduced glutamate content in the substantia nigra following frontal cortex ablation in the rat , 1984, Brain Research.

[82]  C. Carter.  Topographical distribution of possible glutamatergic pathways from the frontal cortex to the striatum and substantia nigra in rats , 1982, Neuropharmacology.

[83]  R. M. Beckstead.  An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat , 1979, The Journal of comparative neurology.

[84]  K. Akert,et al.  Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in macaca fascicularis , 1979, Experimental Brain Research.

[85]  B. Bunney,et al.  The precise localization of nigral afferents in the rat as determined by a retrograde tracing technique , 1976, Brain Research.

[86]  G. Leichnetz,et al.  The efferent projections of the medial prefrontal cortex in the squirrel monkey (Saimiri sciureus) , 1976, Brain Research.

[87]  W. W. Kaelber,et al.  The cortico-nigral fibre tract. An experimental Fink-Heimer study in cats. , 1974, Journal of anatomy.

[88]  J. Carman.  Anatomic basis of surgical treatment of Parkinson's disease. , 1968, The New England journal of medicine.

[89]  E. Rinvik.  The cortico‐nigral projection in the cat an experimental study with silver impregnation methods , 1966, The Journal of comparative neurology.

[90]  G. Giuliani.  [Surgical treatment of dyskinesia]. , 1956, Minerva Medica.

[91]  Timothy Verstynen,et al.  In vivo mapping of microstructural somatotopies in the human corticospinal pathways. , 2011, Journal of neurophysiology.

[92]  F. Calamante,et al.  Effect of step size on probabilistic streamlines : implications for the interpretation of connectivity analyses , 2010 .

[93]  N. Mercuri,et al.  Substantia nigra control of basal ganglia nuclei. , 2009, Journal of neural transmission. Supplementum.

[94]  PhD Atsushi Nambu MD.  A new approach to understand the pathophysiology of Parkinson’s disease , 2005, Journal of Neurology.

[95]  S. T. Sakai.  Corticonigral projections from area 6 in the raccoon , 2004, Experimental Brain Research.

[96]  S. Hyman,et al.  Molecular Neuropharmacology: A Foundation for Clinical Neuroscience , 2001 .

[97]  R. Lehman.  Subthalamic nucleus. , 2000, Journal of neurosurgery.

[98]  M Loyo-Varela,et al.  Pallidotomy in Parkinson's disease. , 1996, Neurosurgery.

[99]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[100]  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.

[101]  J. Talairach,et al.  [Surgical treatment of dyskinesia]. , 1952, Revue neurologique (Paris).

[102]  C. Foix,et al.  Les noyaux gris centraux et la région mésencéphalo-sous-optique : suivi d'un appendice sur l'anatomie pathologique de la maladie parkinson , 2022 .