Identification of a cellular node for motor control pathways

Nature Neuroscience

Volumn 17, Issue 4, 2014, Pages 586-593

  Levine, Ariel J ^a,b   Hinckley, Christopher A ^a,b   Hilde, Kathryn L ^a,b   Driscoll, Shawn P ^a,b   Poon, Tiffany H ^a,b   Montgomery, Jessica M ^a,b   Pfaff, Samuel L ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; FEMALE; MALE; MOTONEURON; MOTOR CONTROL; MOTOR CORTEX; MOUSE; NERVE CELL NETWORK; NERVE STIMULATION; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; REFLEX; SPINAL CORD; VOLUNTARY MOVEMENT;

ANIMALS; EFFERENT PATHWAYS; MICE; MOTOR CORTEX; MOTOR NEURONS; MOVEMENT; MUSCLE, SKELETAL; NERVE NET; NEURAL PATHWAYS; POSTERIOR HORN CELLS; SPINAL CORD;

EID: 84897384168     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3675     Document Type: Article

References (53)

1. Tresch, M.C., Saltiel, P., d'Avella, A. & Bizzi, E. Coordination and localization in spinal motor systems. Brain Res. Rev. 40, 66-79 (2002
2. Bizzi, E., Cheung, V.C., d'Avella, A., Saltiel, P. & Tresch, M. Combining modules for movement. Brain Res. Brain Res. Rev. 57, 125-133 (2008
3. Duysens, J., De Groote, F. & Jonkers, I. The flexion synergy, mother of all synergies and father of new models of gait. Front. Comput. Neurosci. 7, 14 (2013
4. Sherrington, C.S. The Integrative Action of the Nervous System (C. Scribner's Sons, 1906
5. Lundberg, A. Supraspinal control of transmission in reflex paths to motoneurones and primary afferents. Prog. Brain Res. 12, 197-221 (1964
6. Leyton, S. & Sherrington, C.S. Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Q. J. Exp. Physiol. 11, 135-222 (1917
7. Graziano, M.S., Taylor, C.S. & Moore, T. Complex movements evoked by microstimulation of precentral cortex. Neuron 34, 841-851 (2002
8. McHanwell, S. & Biscoe, T.J. The localization of motoneurons supplying the hindlimb muscles of the mouse. Phil. Trans. R. Soc. Lond. B 293, 477-508 (1981
9. Nicolopoulos-Stournaras, S. & Iles, J.F. Motor neuron columns in the lumbar spinal cord of the rat. J. Comp. Neurol. 217, 75-85 (1983
10. de Leon, R., Hodgson, J.A., Roy, R.R. & Edgerton, V.R. Extensor- and flexor-like modulation within motor pools of the rat hindlimb during treadmill locomotion and swimming. Brain Res. 654, 241-250 (1994
11. Wickersham, I.R., Finke, S., Conzelmann, K.K. & Callaway, E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 4, 47-49 (2007
12. Stepien, A.E., Tripodi, M. & Arber, S. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 68, 456-472 (2010
13. Coulon, P., Bras, H. & Vinay, L. Characterization of last-order premotor interneurons by transneuronal tracing with rabies virus in the neonatal mouse spinal cord. J. Comp. Neurol. 519, 3470-3487 (2011
14. Ruigrok, T.J., Pijpers, A., Goedknegt-Sabel, E. & Coulon, P. Multiple cerebellar zones are involved in the control of individual muscles: A retrograde transneuronal tracing study with rabies virus in the rat. Eur. J. Neurosci. 28, 181-200 (2008
15. Scheibel, M.E. & Scheibel, A.B. Terminal axonal patterns in cat spinal cord. II. The dorsal horn. Brain Res. 9, 32-58 (1968
16. Sherrington, C.S. & Laslett, E.E. Observations on some spinal reflexes and the interconnection of spinal segments. J. Physiol. (Lond.) 29, 58-96 (1903
17. Sengul, G., Puchalski, R.B. & Watson, C. Cytoarchitecture of the spinal cord of the postnatal (P4) mouse. Anat. Rec. 295, 837-845 (2012
18. Harrison, P.J., Jankowska, E. & Zytnicki, D. Lamina VIII interneurones interposed in crossed reflex pathways in the cat. J. Physiol. 371, 147-166 (1986
19. Hongo, T., Kitazawa, S., Ohki, Y. & Xi, M.C. Functional identification of last-order interneurones of skin reflex pathways in the cat forelimb segments. Brain Res. 505, 167-170 (1989
20. Puskar, Z. & Antal, M. Localization of last-order premotor interneurons in the lumbar spinal cord of rats. J. Comp. Neurol. 389, 377-389 (1997
21. Asante, C.O. & Martin, J.H. Differential joint-specific corticospinal tract projections within the cervical enlargement. PLoS ONE 8, e74454 (2013
22. Hongo, T., Kitazawa, S., Ohki, Y., Sasaki, M. & Xi, M.C. A physiological and morphological study of premotor interneurones in the cutaneous reflex pathways in cats. Brain Res. 505, 163-166 (1989
23. Tresch, M.C. & Bizzi, E. Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation. Exp. Brain Res. 129, 401-416 (1999
24. Osakada, F. et al. New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. Neuron 71, 617-631 (2011
25. Clarke, R.W. & Harris, J. The organization of motor responses to noxious stimuli. Brain Res. Brain Res. Rev. 46, 163-172 (2004
26. Pierrot-Deseilligny, E. & Burke, D. The Circuitry of the Human Spinal Cord. 350-352 (Cambridge University Press, 2012
27. Schouenborg, J. & Kalliomaki, J. Functional organization of the nociceptive withdrawal reflexes. I. Activation of hindlimb muscles in the rat. Exp. Brain Res. 83, 67-78 (1990
28. Gong, S. et al. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925 (2003
29. Henry, A.M. & Hohmann, J.G. High-resolution gene expression atlases for adult and developing mouse brain and spinal cord. Mammalian Genome 23, 539-549 (2012
30. Wildner, H. et al. Genome-wide expression analysis of Ptf1a- and Ascl1-deficient mice reveals new markers for distinct dorsal horn interneuron populations contributing to nociceptive reflex plasticity. J. Neurosci. 33, 7299-7307 (2013
31. Britanova, O., Akopov, S., Lukyanov, S., Gruss, P. & Tarabykin, V. Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur. J. Neurosci. 21, 658-668 (2005
32. Alaynick, W.A., Jessell, T.M. & Pfaff, S.L. Snapshot: Spinal cord development. Cell. 146, 178 (2011
33. Harrison, T.C., Ayling, O.G. & Murphy, T.H. Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography. Neuron 74, 397-409 (2012
34. Ramanathan, D., Conner, J.M. & Tuszynski, M.H. A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc. Natl. Acad. Sci. USA 103, 11370-11375 (2006
35. Ishizuka, N., Mannen, H., Hongo, T. & Sasaki, S. Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: Three dimensional reconstructions from serial sections. J. Comp. Neurol. 186, 189-211 (1979
36. Scheibel, M.E. & Scheibel, A.B. Terminal patterns in cat spinal cord. 3. Primary afferent collaterals. Brain Res. 13, 417-443 (1969
37. Gianino, S. et al. Postnatal growth of corticospinal axons in the spinal cord of developing mice. Brain Res. Dev. Brain Res. 112, 189-204 (1999
38. Curfs, M.H., Gribnau, A.A. & Dederen, P.J. Selective elimination of transient corticospinal projections in the rat cervical spinal cord gray matter. Brain Res. Dev. Brain Res. 78, 182-190 (1994
39. Martin, J.H. Differential spinal projections from the forelimb areas of the rostral and caudal subregions of primary motor cortex in the cat. Exp. Brain Res. 108, 191-205 (1996
40. Schouenborg, J., Weng, H.R., Kalliomaki, J. & Holmberg, H. A survey of spinal dorsal horn neurones encoding the spatial organization of withdrawal reflexes in the rat. Exp. Brain Res. 106, 19-27 (1995
41. Saltiel, P., Tresch, M.C. & Bizzi, E. Spinal cord modular organization and rhythm generation: An NMDA iontophoretic study in the frog. J. Neurophysiol. 80, 2323-2339 (1998
42. Goulding, M. Circuits controlling vertebrate locomotion: Moving in a new direction. Nat. Rev. Neurosci. 10, 507-518 (2009
43. Bareyre, F.M., Kerschensteiner, M., Misgeld, T. & Sanes, J.R. Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat. Med. 11, 1355-1360 (2005
44. Liang, H., Paxinos, G. & Watson, C. The red nucleus and the rubrospinal projection in the mouse. Brain Struct. Funct. 217, 221-232 (2012
45. Brown, L.T. Rubrospinal projections in the rat. J. Comp. Neurol. 154, 169-187 (1974
46. Antal, M. et al. The termination pattern and postsynaptic targets of rubrospinal fibers in the rat spinal cord: A light and electron microscopic study. J. Comp. Neurol. 325, 22-37 (1992
47. Lundberg, A. Multisensory control of spinal reflex pathways. Prog. Brain Res. 50, 11-28 (1979
48. Schomburg, E.D. Spinal sensorimotor systems and their supraspinal control. Neurosci. Res. 7, 265-340 (1990
49. Barthelemy, D., Leblond, H., Provencher, J. & Rossignol, S. Nonlocomotor and locomotor hindlimb responses evoked by electrical microstimulation of the lumbar cord in spinalized cats. J. Neurophysiol. 96, 3273-3292 (2006
50. Mushahwar, V.K., Aoyagi, Y., Stein, R.B. & Prochazka, A. Movements generated by intraspinal microstimulation in the intermediate gray matter of the anesthetized, decerebrate, and spinal cat. Can. J. Physiol. Pharmacol. 82, 702-714 (2004
51. Wickersham, I.R., Sullivan, H.A. & Seung, H.S. Production of glycoprotein-deleted rabies viruses for monosynaptic tracing and high-level gene expression in neurons. Nat. Protoc. 5, 595-606 (2010
52. Joshi, P.S. et al. Bhlhb5 regulates the postmitotic acquisition of area identities in layers II-V of the developing neocortex. Neuron 60, 258-272 (2008
53. Cheng, L. et al. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 7, 510-517 (2004