Motor-circuit communication matrix from spinal cord to brainstem neurons revealed by developmental origin

Cell

Volumn 156, Issue 3, 2014, Pages 537-548

  Pivetta, Chiara ^a,b   Esposito, Maria Soledad ^a,b   Sigrist, Markus ^a,b   Arber, Silvia ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER; CRE RECOMBINASE; RECOMBINASE;

ANIMAL CELL; ARTICLE; CELL SUBPOPULATION; CERVICAL SPINE; FORELIMB; GENETICS; INTERNEURON; LATERAL RETICULAR NUCLEUS; MOTONEURON; MOTOR ACTIVITY; MOTOR CONTROL; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RABIES VIRUS; SPINAL CORD; SPINAL CORD NERVE CELL; STEM CELL; SYNAPTIC TRANSMISSION; CERVICAL SPINAL CORD; CONNECTOME; CONTROLLED STUDY; CUNEATE NUCLEUS; PONTINE NUCLEUS; THORACIC SPINAL CORD; TRANSIENT EXPRESSION;

ANIMALS; AXONS; BRAIN STEM; GENETIC TECHNIQUES; MICE; MICE, TRANSGENIC; MOTOR NEURONS; NEURAL PATHWAYS; NEURONS; NEUROTRANSMITTER AGENTS; SPINAL CORD; SYNAPSES;

EID: 84893431312     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.014     Document Type: Article

References (63)

1. W.A. Alaynick, T.M. Jessell, and S.L. Pfaff SnapShot: spinal cord development Cell 146 2011 178-178, e1
2. B. Alstermark, and T. Isa Circuits for skilled reaching and grasping Annu. Rev. Neurosci. 35 2012 559 578
3. B. Alstermark, A. Lundberg, and S. Sasaki Integration in descending motor pathways controlling the forelimb in the cat. 10. Inhibitory pathways to forelimb motoneurones via C3-C4 propriospinal neurones Exp. Brain Res. 56 1984 279 292
4. B. Alstermark, M.J. Pinter, and S. Sasaki Pyramidal effects in dorsal neck motoneurones of the cat J. Physiol. 363 1985 287 302
5. B. Alstermark, T. Isa, and B. Tantisira Integration in descending motor pathways controlling the forelimb in the cat. 18. Morphology, axonal projection and termination of collaterals from C3-C4 propriospinal neurones in the segment of origin Exp. Brain Res. 84 1991 561 568
6. B. Alstermark, T. Isa, L.G. Pettersson, and S. Sasaki The C3-C4 propriospinal system in the cat and monkey: a spinal pre-motoneuronal centre for voluntary motor control Acta Physiol. (Oxf.) 189 2007 123 140
7. S. Arber Motor circuits in action: specification, connectivity, and function Neuron 74 2012 975 989
8. Y.I. Arshavsky, I.M. Gelfand, and G.N. Orlovsky Cerebellum and Rhythmical Movements 1986 Springer Berlin
9. Y.I. Arshavsky, I.M. Gelfand, G.N. Orlovsky, and G.A. Pavlova Messages conveyed by spinocerebellar pathways during scratching in the cat. I. Activity of neurons of the lateral reticular nucleus Brain Res. 151 1978 479 491
10. E. Azim, J. Jiang, B. Alstermark, and T.M. Jessell Skilled reaching relies on a V2a propriospinal internal copy circuit Nature 2014 10.1038/nature13021 Published online February 2, 2014
11. A. Brodal Spinal afferents to the lateral reticular nucleus of the medulla oblongata in the cat; an experimental study J. Comp. Neurol. 91 1949 259 295
12. T.V. Bui, T. Akay, O. Loubani, T.S. Hnasko, T.M. Jessell, and R.M. Brownstone Circuits for grasping: spinal dI3 interneurons mediate cutaneous control of motor behavior Neuron 78 2013 191 204
13. S.K. Campbell, T.D. Parker, and W. Welker Somatotopic organization of the external cuneate nucleus in albino rats Brain Res. 77 1974 1 23
14. M. Clendenin, C.F. Ekerot, O. Oscarsson, and I. Rosén The lateral reticular nucleus in the cat. I. Mossy fibre distribution in cerebellar cortex Exp. Brain Res. 21 1974 473 486
15. M. Clendenin, C.F. Ekerot, O. Oscarsson, and I. Rosén The lateral reticular nucleus in the cat. II. Organization of component activated from bilateral ventral flexor reflex tract (bVFRT) Exp. Brain Res. 21 1974 487 500
16. T.B. Crapse, and M.A. Sommer Corollary discharge across the animal kingdom Nat. Rev. Neurosci. 9 2008 587 600
17. C.F. Ekerot The lateral reticular nucleus in the cat. VIII. Excitatory and inhibitory projection from the bilateral ventral flexor reflex tract (bVFRT) Exp. Brain Res. 79 1990 129 137
18. K. Ezure, and I. Tanaka Convergence of central respiratory and locomotor rhythms onto single neurons of the lateral reticular nucleus Exp. Brain Res. 113 1997 230 242
19. M. Goulding Circuits controlling vertebrate locomotion: moving in a new direction Nat. Rev. 10 2009 507 518
20. S. Grillner, and T.M. Jessell Measured motion: searching for simplicity in spinal locomotor networks Curr. Opin. Neurobiol. 19 2009 572 586
21. A. Hinman, and M.B. Carpenter Efferent fiber projections of the red nucleus in the cat J. Comp. Neurol. 113 1959 61 82
22. S. Hippenmeyer, E. Vrieseling, M. Sigrist, T. Portmann, C. Laengle, D.R. Ladle, and S. Arber A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol. 3 2005 e159
23. M. Ito Cerebellar circuitry as a neuronal machine Prog. Neurobiol. 78 2006 272 303
24. E. Jankowska, and I. Hammar Interactions between spinal interneurons and ventral spinocerebellar tract neurons J. Physiol. 591 2013 5445 5451
25. E. Jankowska, P. Krutki, and I. Hammar Collateral actions of premotor interneurons on ventral spinocerebellar tract neurons in the cat J. Neurophysiol. 104 2010 1872 1883
26. O. Kiehn Development and functional organization of spinal locomotor circuits Curr. Opin. Neurobiol. 21 2011 100 109
27. S.K. Koekkoek, and T.J. Ruigrok Lack of a bilateral projection of individual spinal neurons to the lateral reticular nucleus in the rat: a retrograde, non-fluorescent, double labeling study Neurosci. Lett. 200 1995 13 16
28. H. Künzle The topographic organization of spinal afferents to the lateral reticular nucleus of the cat J. Comp. Neurol. 149 1973 103 115
29. A. Lundberg Function of the ventral spinocerebellar tract. A new hypothesis Exp. Brain Res. 12 1971 317 330
30. G.N. Orlovsky, T.G. Deliagina, and S. Grillner Neuronal Control of Locomotion: From Mollusc to Man 1999 Oxford University Press Oxford
31. O. Oscarsson Functional organization of the spino- and cuneocerebellar tracts Physiol. Rev. 45 1965 495 522
32. G. Paxinos, and K.B. Franklin The Mouse Brain in Stereotaxic Coordinates 4th edition 2012 Elsevier San Diego
33. J.F. Poulet, and B. Hedwig New insights into corollary discharges mediated by identified neural pathways Trends Neurosci. 30 2007 14 21
34. N. Rajakumar, A.W. Hrycyshyn, and B.A. Flumerfelt Afferent organization of the lateral reticular nucleus in the rat: an anterograde tracing study Anat. Embryol. (Berl.) 185 1992 25 37
35. I. Rosén Localization in caudal brain stem and cervical spinal cord of neurones activated from forelimb group I afferents in the cat Brain Res. 16 1969 55 71
36. E. Santarcangelo, O. Pompeiano, and G. Stampacchia Effects of kainic acid lesions of lateral reticular nucleus on posture and reflex movements Arch. Ital. Biol. 119 1981 324 340
37. S. Shakya Shrestha, B.A. Bannatyne, E. Jankowska, I. Hammar, E. Nilsson, and D.J. Maxwell Inhibitory inputs to four types of spinocerebellar tract neurons in the cat spinal cord Neuroscience 226 2012 253 269
38. S.S. Shrestha, B.A. Bannatyne, E. Jankowska, I. Hammar, E. Nilsson, and D.J. Maxwell Excitatory inputs to four types of spinocerebellar tract neurons in the cat and the rat thoraco-lumbar spinal cord J. Physiol. 590 2012 1737 1755
39. Y. Shinoda, I. Sugihara, H.S. Wu, and Y. Sugiuchi The entire trajectory of single climbing and mossy fibers in the cerebellar nuclei and cortex Prog. Brain Res. 124 2000 173 186
40. M.T. Shokunbi, A.W. Hrycyshyn, and B.A. Flumerfelt Spinal projections to the lateral reticular nucleus in the rat: a retrograde labelling study using horseradish peroxidase J. Comp. Neurol. 239 1985 216 226
41. M.A. Sommer, and R.H. Wurtz Brain circuits for the internal monitoring of movements Annu. Rev. Neurosci. 31 2008 317 338
42. A.E. Stepien, M. Tripodi, and S. Arber Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells Neuron 68 2010 456 472
43. M. Tripodi, A.E. Stepien, and S. Arber Motor antagonism exposed by spatial segregation and timing of neurogenesis Nature 479 2011 61 66
44. G. Ugolini Advances in viral transneuronal tracing J. Neurosci. Methods 194 2010 2 20
45. L. Vong, C. Ye, Z. Yang, B. Choi, S. Chua Jr.; and B.B. Lowell Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons Neuron 71 2011 142 154
46. F. Walberg Descending connections to the lateral reticular nucleus; an experimental study in the cat J. Comp. Neurol. 109 1958 363 389
47. I.R. Wickersham, D.C. Lyon, R.J. Barnard, T. Mori, S. Finke, K.K. Conzelmann, J.A. Young, and E.M. Callaway Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons Neuron 53 2007 639 647
48. D.M. Wolpert, and R.C. Miall Forward models for physiological motor control Neural Netw. 9 1996 1265 1279
49. H.S. Wu, I. Sugihara, and Y. Shinoda Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei J. Comp. Neurol. 411 1999 97 118
50. Y. Zhang, S. Narayan, E. Geiman, G.M. Lanuza, T. Velasquez, B. Shanks, T. Akay, J. Dyck, K. Pearson, and S. Gosgnach et al. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking Neuron 60 2008 84 96
51. S. Hippenmeyer, E. Vrieseling, M. Sigrist, T. Portmann, C. Laengle, D.R. Ladle, and S. Arber A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol. 3 2005 e159
52. E.J. Kremer, S. Boutin, M. Chillon, and O. Danos Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer J. Virol. 74 2000 505 512
53. E. Pecho-Vrieseling, M. Sigrist, Y. Yoshida, T.M. Jessell, and S. Arber Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition Nature 459 2009 842 846
54. C.Y. Peng, H. Yajima, C.E. Burns, L.I. Zon, S.S. Sisodia, S.L. Pfaff, and K. Sharma Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord Neuron 53 2007 813 827
55. T. Sapir, E.J. Geiman, Z. Wang, T. Velasquez, S. Mitsui, Y. Yoshihara, E. Frank, F.J. Alvarez, and M. Goulding Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development J. Neurosci. 24 2004 1255 1264
56. K. Sharma, H.Z. Sheng, K. Lettieri, H. Li, A. Karavanov, S. Potter, H. Westphal, and S.L. Pfaff LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons Cell 95 1998 817 828
57. S. Srinivas, T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev. Biol. 1 2001 4
58. A.E. Stepien, M. Tripodi, and S. Arber Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells Neuron 68 2010 456 472
59. M. Tripodi, A.E. Stepien, and S. Arber Motor antagonism exposed by spatial segregation and timing of neurogenesis Nature 479 2011 61 66
60. L. Vong, C. Ye, Z. Yang, B. Choi, S. Chua Jr.; and B.B. Lowell Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons Neuron 71 2011 142 154
61. I.R. Wickersham, H.A. Sullivan, and H.S. Seung Production of glycoprotein-deleted rabies viruses for monosynaptic tracing and high-level gene expression in neurons Nat. Protoc. 5 2010 595 606
62. H.U. Zeilhofer, B. Studler, D. Arabadzisz, C. Schweizer, S. Ahmadi, B. Layh, M.R. Bösl, and J.M. Fritschy Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice J. Comp. Neurol. 482 2005 123 141
63. Y. Zhang, S. Narayan, E. Geiman, G.M. Lanuza, T. Velasquez, B. Shanks, T. Akay, J. Dyck, K. Pearson, and S. Gosgnach et al. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking Neuron 60 2008 84 96