A direct cortico-nigral pathway as revealed by constrained spherical deconvolution tractography in humans

Frontiers in Human Neuroscience

Volumn 10, Issue , 2016, Pages

  Cacciola, Alberto ^a   Milardi, Demetrio ^a,b   Anastasi, Giuseppe P ^a   Basile, Gianpaolo A ^a   Ciolli, Pietro ^a   Irrera, Mariangela ^a   Cutroneo, Giuseppina ^a   Bruschetta, Daniele ^a   Rizzo, Giuseppina ^a   Mondello, Stefania ^a   Bramanti, Placido ^b   Quartarone, Angelo ^a,b  

^a UNIVERSITY OF MESSINA   (Italy)

^b IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

Author keywords

Basal ganglia; Connectivity; Cortex; CSD; Parkinson disease; Substantia nigra; Tractography

Indexed keywords

ADDICTION; ADULT; ARTICLE; BRAIN CORTEX; CONSTRAINED SPHERICAL DECONVOLUTION TRACTOGRAPHY; DIFFUSION TENSOR IMAGING; FEMALE; HUMAN; HUMAN EXPERIMENT; IMAGE SEGMENTATION; IN VIVO STUDY; MALE; NORMAL HUMAN; PARKINSON DISEASE; PATHOPHYSIOLOGY; POSTCENTRAL GYRUS; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; SCHIZOPHRENIA; SUBSTANTIA NIGRA; SUPERIOR PARIETAL LOBULE; TRACTOGRAPHY;

EID: 84983801012     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fncel.2016.00374     Document Type: Article

References (96)

1. Afifi, A. K., Bahuth, N. B., Kaelber, W. W., Mikhael, E., and Nassar, S. (1974). The cortico-nigral fibre tract.An experimental Fink-Heimer study in cats. J. Anat. 118, 469-476.
2. Alexander, D. C., and Barker, G. J. (2005). Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 27, 357-367. doi: 10.1016/j.neuroimage.2005.04.008
3. Basser, P. J. (1995). Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8, 333-344. doi: 10.1002/nbm.1940080707
4. Basser, P. J., Mattiello, J., and LeBihan, D. (1994). MR diffusion tensor spectroscopy and imaging. Biophys. J. 66, 259-267. doi: 10.1016/S0006-3495(94)80775-1
5. Bateup, H. S., Santini, E., Shen, W., Birnbaum, S., Valjent, E., Surmeier, D. J., et al. (2010). Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc. Natl. Acad. Sci. U.S.A. 107, 14845-14850. doi: 10.1073/pnas.1009874107
6. Beckstead, R. M. (1979). An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J. Comp. Neurol. 184, 43-62. doi: 10.1002/cne.901840104
7. Behrens, T. E., Berg, H. J., Jbabdi, S., Rushworth, M. F., and Woolrich, M. W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34, 144-155. doi: 10.1016/j.neuroimage.2006.09.018
8. Behrens, T. E., and Sporns, O. (2012). Human connectomics. Curr. Opin. Neurobiol. 22, 144-153. doi: 10.1016/j.conb.2011.08.005
9. Bejjani, B., Damier, P., Arnulf, I., Bonnet, A. M., Vidailhet, M., Dormont, D., et al. (1997). Pallidal stimulation for Parkinson's disease. Two targets? Neurology 49, 1564-1569. doi: 10.1212/WNL.49.6.1564
10. Besson, P., Dinkelacker, V., Valabregue, R., Thivard, L., Leclerc, X., Baulac, M., et al. (2014). Structural connectivity differences in left and right temporal lobe epilepsy. Neuroimage 100, 135-144. doi: 10.1016/j.neuroimage.2014.04.071
11. Bijttebier, S., Caeyenberghs, K., van den Ameele, H., Achten, E., Rujescu, D., Titeca, K., et al. (2015). The vulnerability to suicidal behavior is associated with reduced connectivity strength. Front. Hum. Neurosci. 9:632. doi: 10.3389/fnhum.2015.00632
12. Bosch, C., Degos, B., Deniau, J. M., and Venance, L. (2011). Subthalamic nucleus high-frequency stimulation generates a concomitant synaptic excitation-inhibition in substantia nigra pars reticulata. J. Physiol. 589(Pt 17), 4189-4207. doi: 10.1113/jphysiol.2011.211367
13. Bunney, B. S., and Aghajanian, G. K. (1976). The precise localization of nigral afferents in the rat as determined by a retrograde tracing technique. Brain Res. 117, 423-435. doi: 10.1016/0006-8993(76)90751-4
14. Cacciola, A., Milardi, D., and Quartarone, A. (2016). Role of cortico-pallidal connectivity in the pathophysiology of dystonia. Brain. doi: 10.1093/brain/aww102. [Epub ahead of print].
15. Carman, J. B. (1968). Anatomic basis of surgical treatment of Parkinson's disease. N. Engl. J. M. 17, 919-930. doi: 10.1056/NEJM196810242791706
16. Carter, C. J. (1982). Topographical distribution of possible glutamatergic pathways from the frontal cortex to the striatum and substantia nigra in rats. Neuropharmacology 21, 379-383. doi: 10.1016/0028-3908(82)90019-3
17. Cheng, H., Wang, Y., Sheng, J., Kronenberger, W. G., Mathews, V. P., Hummer, T. A., et al. (2012). Characteristics and variability of structural networks derived from diffusion tensor imaging. Neuroimage 61, 1153-1164. doi: 10.1016/j.neuroimage.2012.03.036
18. Chowdhury, R., Lambert, C., Dolan, R. J., and Düzel, E. (2013). Parcellation of the human substantia nigra based on anatomical connectivity to the striatum. Neuroimage 81, 191-198. doi: 10.1016/j.neuroimage.2013.05.043
19. Chung, H. W., Chou, M. C., and Chen, C. Y. (2011). Principles and limitations of computational algorithms in clinical diffusion tensor MR tractography. Am. J. Neuroradiol. 32, 3-13. doi: 10.3174/ajnr.A2041
20. DeLong, M. R. (1990). Primate models of movement disorders of basal ganglia origin. Trends. Neurosci. 13, 281-285. doi: 10.1016/0166-2236(90)90110-V
21. Descoteaux, M., Deriche, R., Knösche, T. R., and Anwander, A. (2009). Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans. Med. Imaging. 28, 269-286. doi: 10.1109/TMI.2008.2004424
22. Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980. doi: 10.1016/j.neuroimage.2006.01.021
23. Draganski, B., Kherif, F., Klöppel, S., Cook, P. A., Alexander, D. C., Parker, G. J., et al. (2008). Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J. Neurosci. 28, 7143-7152. doi: 10.1523/JNEUROSCI.1486-08.2008
24. Düzel, E., Bunzeck, N., Guitart-Masip, M., Wittmann, B., Schott, B. H., and Tobler, P. N. (2009). Functional imaging of the human dopaminergic midbrain. Trends Neurosci. 32, 321-328. doi: 10.1016/j.tins.2009.02.005
25. Dybdal, D., Forcelli, P. A., Dubach, M., Oppedisano, M., Holmes, A., Malkova, L., et al. (2013). Topography of dyskinesias and torticollis evoked by inhibition of substantia nigra pars reticulate. Mov. Disord. 28, 460-468. doi: 10.1002/mds.25215
26. Embleton, K. V., Haroon, H. A., Morris, D. M., Ralph, M. A., and Parker, G. J. (2010). Distortion correction for diffusion-weighted MRI tractography and fMRI in the temporal lobes. Hum. Brain Mapp. 31, 1570-1587. doi: 10.1002/hbm.20959
27. Farquharson, S., Tournier, J. D., Calamante, F., Fabinyi, G., Schneider-Kolsky, M., Jackson, G. D., et al. (2013). White matter fiber tractography: why we need to move beyond DTI. J. Neurosurg. 118, 1367-1377. doi: 10.3171/2013.2.JNS121294
28. Fillard, P., Descoteaux, M., Goh, A., Gouttard, S., Jeurissen, B., Malcolm, J., et al. (2011). Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 56, 220-234. doi: 10.1016/j.neuroimage.2011.01.032
29. Fischl, B., and Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U.S.A. 97, 11050-11055. doi: 10.1073/pnas.200033797
30. Fischl, B., Salat, D. H., van der Kouwe, A. J., Makris, N., Ségonne, F., Quinn, B. T., et al. (2004). Sequence-independent segmentation of magnetic resonance images. Neuroimage 23(Suppl. 1), S69-S84. doi: 10.1016/j.neuroimage.2004.07.016
31. Foix, C., and Niculescu, I. T. (1925). Anatomie Cérébrale; Les Noyaux Gris Centraux et la Région Mésencéphalo-Sous-Optique, Suivi d'un Appendice sur L'anatomie Pathologique de la Maladie de Parkinson. Paris: Masson et cie.
32. Frankle, W. G., Laruelle, M., and Haber, S. N. (2006). Prefrontal cortical projections to the midbrain in primates: evidence for a sparse connection. Neuropsychopharmacology 31, 1627-1636. doi: 10.1038/sj.npp.1300990
33. Gariano, R. F., and Groves, P. M. (1988). Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res. 462, 194-198. doi: 10.1016/0006-8993(88)90606-3
34. Grèzes, J., Valabrègue, R., Gholipour, B., and Chevallier, C. (2014). A direct amygdala-motor pathway for emotional displays to influence action: a diffusion tensor imaging study. Hum. Brain Mapp. 35, 5974-5983. doi: 10.1002/hbm.22598
35. Guatteo, E., Cucchiaroni, M. L., and Mercuri, N. B. (2009). Substantia nigra control of basal ganglia nuclei. J. Neural Transm. Suppl. 73, 91-101. doi: 10.1007/978-3-211-92660-4_7
36. Guridi, J., and Lozano, A. M. (1997). A brief history of pallidotomy. Neurosurgery 41, 1169-1180. doi: 10.1097/00006123-199711000-00029
37. Henderson, J. M. (2012). “Connectomic surgery”: diffusion tensor imaging (DTI) tractography as a targeting modality for surgical modulation of neural networks. Front. Integr. Neurosci. 6:15. doi: 10.3389/fnint.2012.00015
38. Höglinger, G. U., Alvarez-Fischer, D., Arias-Carrión, O., Djufri, M., Windolph, A., Keber, U., et al. (2015). A new dopaminergic nigro-olfactory projection. Acta Neuropathol. 130, 333-348. doi: 10.1007/s00401-015-1451-y
39. Jang, S. H., Son, S. M., Lee, D. Y., and Hong, J. H. (2013). Relationship between somatosensory function and the spinothalamocortical pathway in chronic stroke patients. Somatosens. Mot. Res. 30, 197-200. doi: 10.3109/08990220.2013.790808
40. Jasmin, L., Granato, A., and Ohara, P. T. (2004). Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J. Comp.Neurol. 468, 425-440. doi: 10.1002/cne.10978
41. Jbabdi, S., and Johansen-Berg, H. (2011). Tractography: where do we go from here? Brain Connect. 1, 169-183. doi: 10.1089/brain.2011.0033
42. Jbabdi, S., Sotiropoulos, S. N., Haber, S. N., Van Essen, D. C., and Behrens, T. E. (2015). Measuring macroscopic brain connections in vivo. Nat. Neurosci. 18, 1546-1555. doi: 10.1038/nn.4134
43. Jeurissen, B., Leemans, A., Tournier, J. D., Jones, D. K., and Sijbers, J. (2013). Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum. Brain Mapp. 34, 2747-2766. doi: 10.1002/hbm.22099
44. Jones, D. K., and Basser, P. J. (2004). “Squashing peanuts and smashing pumpkins”: how noise distorts diffusion-weighted MR data. Magn. Reson. Med. 52, 979-993. doi: 10.1002/mrm.20283
45. Jones, D. K., and Cercignani, M. (2010). Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 23, 803-820. doi: 10.1002/nbm.1543
46. Kita, H. (2001). Neostriatal and globus pallidus stimulation induced inhibitory postsynaptic potentials in entopeduncular neurons in rat brain slice preparations. Neuroscience 105, 871-879. doi: 10.1016/S0306-4522(01)00231-7
47. Kornhuber, J. (1984). The cortico-nigral projection: reduced glutamate content in the substantia nigra following frontal cortex ablation in the rat. Brain Res. 322, 124-126. doi: 10.1016/0006-8993(84)91189-2
48. Künzle, H. (1978). An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. Brain Behav. Evol. 15, 185-234. doi: 10.1159/000123779
49. Kwon, H. G., and Jang, S. H. (2014). Differences in neural connectivity between the substantia nigra and ventral tegmental area in the human brain. Front. Hum. Neurosci. 8:41. doi: 10.3389/fnhum.2014.00041
50. Lambert, C., Zrinzo, L., Nagy, Z., Lutti, A., Hariz, M., Foltynie, T., et al. (2012). Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage 60, 83-94 doi: 10.1016/j.neuroimage.2011.11.082
51. Le Bihan, D., and Johansen-Berg, H. (2012). Diffusion MRI at 25: exploring brain tissue structure and function. Neuroimage 61, 324-341 doi: 10.1016/j.neuroimage.2011.11.006
52. Leblois, A., Boraud, T., Meissner, W., Bergman, H., and Hansel, D. (2006). Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci. 26, 3567-3583. doi: 10.1523/JNEUROSCI.5050-05.2006
53. Leichnetz, G. R., and Astruc, J. (1976). The efferent projections of the medial prefrontal cortex in the squirrel monkey (Saimiri sciureus). Brain Res. 109, 455-472. doi: 10.1016/0006-8993(76)90027-5
54. Li, C., Huang, B., Zhang, R., Ma, Q., Yang, W., Wang, L., et al. (2016). Impaired topological architecture of brain structural networks in idiopathic Parkinson's disease: a DTI study. Brain Imaging Behav. doi: 10.1007/s11682-015-9501-6. [Epub ahead of print].
55. Lozano, A. M., and Lang, A. E. (2001). Pallidotomy for Parkinson's disease. Adv. Neurol. 86, 413-420.
56. McFarland, N. R., and Haber, S. N. (2000). Convergent inputs from thalamic motor nuclei and frontal cortical areas to the dorsal striatum in the primate. J. Neurosci. 20, 3798-3813.
57. Menke, R. A., Jbabdi, S., Miller, K. L., Matthews, P. M., and Zarei, M. (2010). Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson's disease. Neuroimage 52, 1175-1180. doi: 10.1016/j.neuroimage.2010.05.086
58. Milardi, D., Arrigo, A., Anastasi, G., Cacciola, A., Marino, S., Mormina, E., et al. (2016a). Extensive direct subcortical cerebellum-basal ganglia connections in human brain as revealed by constrained spherical deconvolution tractography. Front. Neuroanat. 10:29. doi: 10.3389/fnana.2016.00029
59. Milardi, D., Cacciola, A., Cutroneo, G., Marino, S., Irrera, M., Cacciola, G., et al. (2016b). Red nucleus connectivity as revealed by constrained spherical deconvolution tractography. Neurosci. Lett. 626, 68-73. doi: 10.1016/j.neulet.2016.05.009
60. Milardi, D., Gaeta, M., Marino, S., Arrigo, A., Vaccarino, G., Mormina, E., et al. (2015). Basal ganglia network by constrained spherical deconvolution: a possible cortico-pallidal pathway? Mov. Disord. 30, 342-349. doi: 10.1002/mds.25995
61. Mori, S., Wakana, S., and Van Zijl, P. C. M. (2004). MRI Atlas of Human White Matter. Amsterdam, San Diego, CA: Elsevier.
62. Mormina, E., Arrigo, A., Calamuneri, A., Granata, F., Quartarone, A., Ghilardi, M. F., et al. (2015). Diffusion tensor imaging parameters' changes of cerebellar hemispheres in Parkinson's disease. Neuroradiology 57, 327-334. doi: 10.1007/s00234-014-1473-5
63. Munhoz, R. P., Cerasa, A., and Okun, M. S. (2014). Surgical treatment of dyskinesia in Parkinson's disease. Front. Neurol. 5:65. doi: 10.3389/fneur.2014.00065
64. Naito, A., and Kita, H. (1994). The cortico-nigral projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res. 637, 317-322. doi: 10.1016/0006-8993(94)91252-1
65. Nambu, A. (2005). A new approach to understand the pathophysiology of Parkinson's disease. J. Neurol. 252(Suppl. 4), IV1-IV4. doi: 10.1007/s00415-005-4002-y
66. Nambu, A., Takada, M., Inase, M., and Tokuno, H. (1996). 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. J. Neurosci. 16, 2671-2683.
67. Nambu, A., Tokuno, H., Hamada, I., Kita, H., Imanishi, M., Akazawa, T., et al. (2000). Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84, 289-300.
68. Nambu, A., Tokuno, H., and Takada, M. (2002). Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci. Res. 43, 111-117. doi: 10.1016/S0168-0102(02)00027-5
69. Nestler, E. J., Hyman, S. E., and Malenka, R. C. (2009). Molecular Neuropharmacology: A Foundation for Clinical Neuroscience. New York, NY: McGraw-Hill Medical.
70. Neumann, W. J., Jha, A., Bock, A., Huebl, J., Horn, A., Schneider, G. H., et al. (2015). Cortico-pallidal oscillatory connectivity in patients with dystonia. Brain 138, 1894-1906. doi: 10.1093/brain/awv109
71. Pajevic, S., and Pierpaoli, C. (1999). Colour schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn. Reson. Med. 42, 526-540.
72. Parker, G. D., Marshall, D., Rosin, P. L., Drage, N., Richmond, S., and Jones, D. K. (2013). A pitfall in the reconstruction of fibre ODfs using spherical deconvolution of diffusion MRI data. Neuroimage 65, 433-448. doi: 10.1016/j.neuroimage.2012.10.022
73. Parker, G. J., and Alexander, D. C. (2005). Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360, 893-902. doi: 10.1098/rstb.2005.1639
74. Reuter, M., Rosas, H. D., and Fischl, B. (2010). Highly accurate inverse consistent registration: a robust approach. Neuroimage 53, 1181-1196. doi: 10.1016/j.neuroimage.2010.07.020
75. Rinvik, E. (1966). The cortico-nigral projection in the cat. Brain Res. 126, 241-254.
76. Sakai, S. T. (1978). Corticonigral projections from area 6 in the raccoon. Exp. Brain Res. 73, 498-504. doi: 10.1007/BF00406607
77. Segonne, F., Dale, A. M., Busa, E., Glessner, M., Salat, D., Hahn, H. K., et al. (2004). A hybrid approach to the skull stripping problem in MRI. Neuroimage 22, 1060-1075. doi: 10.1016/j.neuroimage.2004.03.032
78. Ségonne, F., Pacheco, J., and Fischl, B. (2007). Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans. Med. Imaging 26, 518-529. doi: 10.1109/TMI.2006.887364
79. Sesack, S. R., Deutch, A. Y., Roth, R. H., and Bunney, B. S. (1989). Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290, 213-242. doi: 10.1002/cne.902900205
80. Smith, R. E., Tournier, J. D., Calamante, F., and Connelly, A. (2013). SIFT: spherical-deconvolution informed filtering of tractograms. Neuroimage 67, 298-312. doi: 10.1016/j.neuroimage.2012.11.049
81. Smith, Y., and Wichmann, T. (2015). The cortico-pallidal projection: an additional route for cortical regulation of the basal ganglia circuitry. Mov. Disord. M 30, 293-295. doi: 10.1002/mds.26095
82. Strafella, A. P., Paus, T., Barrett, J., and Dagher, A. (2001). Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J. Neurosci. 21, RC157.
83. Testut, L., and Latarjet, A. (1971). Anatomia Umana. Vol. 3. Torino: UTET.
84. Tournier, J. D., Calamante, F., and Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35, 1459-1472. doi: 10.1016/j.neuroimage.2007.02.016
85. Tournier, J. D., Calamante, F., and Connelly, A. (2011). Effect of step size on probabilistic streamlines: implications for the interpretation of connectivity analysis. Proc. Intl. Soc. Mag Reson. Med. 19, 2019.
86. Tournier, J. D., Yeh, C. H., Calamante, F., Cho, K. H., Connelly, A., and Lin, C. P. (2008). Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42, 617-625. doi: 10.1016/j.neuroimage.2008.05.002
87. Verstynen, T., Jarbo, K., Pathak, S., and Schneider, W. (2011). In vivo mapping of microstructural somatotopies in the human corticospinal pathways. J. Neurophysiol. 105, 336-346. doi: 10.1152/jn.00698.2010
88. Volkmann, J., Herzog, J., Kopper, F., and Deuschl, G. (2002). Introduction to the programming of deep brain stimulators. Mov. Disord. 17, S181-S187. doi: 10.1002/mds.10162
89. von Monakow, K. H., Akert, K., and Künzle, H. (1979). Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularis. Exp. Brain Res. 34, 91-105. doi: 10.1007/BF00238343
90. Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W., and Pennartz, C. M. (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468-474. doi: 10.1016/j.tins.2004.06.006
91. Weinberger, D. R. (1987). Implications of the normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry 44, 660-669. doi: 10.1001/archpsyc.1987.01800190080012
92. Wise, R. A. (2009). Roles for nigrostriatal-not just mesocorticolimbic-dopamine in reward and addiction. Trends Neurosci. 32, 517-524. doi: 10.1016/j.tins.2009.06.004
93. Wu, Y. R., Levy, R., Ashby, P., Tasker, R. R., and Dostrovsky, J. O. (2001). Does stimulation of the GPi control dyskinesia by activating inhibitory axons? Mov. Disord. 16, 208-216. doi: 10.1002/mds.1046
94. Zakiewicz, I. M., Bjaalie, J. G., and Leergaard, T. B. (2014). Brain-wide map of efferent projections from rat barrel cortex. Front. Neuroinform. 8:5. doi: 10.3389/fninf.2014.00005
95. Zhang, H. Y., Tang, H., Chen, W. X., Ji, G. J., Ye, J., Wang, N., et al. (2015). Mapping the functional connectivity of the substantia nigra, red nucleus and dentate nucleus: a network analysis hypothesis associated with the extrapyramidal system. Neurosci. Lett. 606, 36-41. doi: 10.1016/j.neulet.2015.08.029
96. Zhou, F. M., and Lee, C. R. (2011). Intrinsic and integrative properties of substantia nigra pars reticulata neurons. Neuroscience 198, 69-94. doi: 10.1016/j.neuroscience.2011.07.061