Glutamatergic reticulospinal neurons in the mouse: Developmental origins, axon projections, and functional connectivity

Annals of the New York Academy of Sciences

Volumn 1279, Issue 1, 2013, Pages 80-89

  Perreault, Marie Claude ^a   Glover, Joel C ^b  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Commissural interneurons; Descending motor control; Motoneurons; Reticular formation; Spinal cord; Voluntary movement

Indexed keywords

ARTICLE; ARTIFICIAL NEURAL NETWORK; BRAIN FUNCTION; EMBRYO DEVELOPMENT; GLUTAMATERGIC RETICULOSPINAL NEURON; HINDLIMB; INTERNEURON; LUMBAR VERTEBRA; MAMMAL; MOTONEURON; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVE FIBER; NERVE FIBER MEMBRANE POTENTIAL; NONHUMAN; POSTNATAL DEVELOPMENT; RETICULAR FORMATION; SPINAL CORD; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; VOLUNTARY MOVEMENT; WAVEFORM;

EID: 84875591764     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12054     Document Type: Article

References (73)

1. Armstrong, D.M. 1988. The supraspinal control of mammalian locomotion. J. Physiol. 405: 1-37.
2. Jordan, L.M. 1998. Initiation of locomotion in mammals. Ann. N.Y. Acad. Sci. 860: 83-93.
3. Guyenet, P.G. 2006. The sympathetic control of blood pressure. Nat. Rev. 7: 335-346.
4. Schepens, B., P. Stapley & T. Drew . 2008. Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. J. Neurophysiol. 100: 2235-2253.
5. Davidson, A.G. & J.A. Buford . 2006. Bilateral actions of the reticulospinal tract on arm and shoulder muscles In the monkey: stimulus triggered averaging. Exp. Brain Res. 173: 25-39.
6. Pettersson, L.-G. et al. 2007. Skilled digit movements in feline and primate-recovery after selective spinal cord lesions. Acta Physiol. 189: 141-154.
7. Soteropoulos, D., E.R. Williams & S.N. Baker . 2012. Cells in the monkey ponto-medullary reticular formation modulate their activity with slow finger movements. J. Physiol. 590: 4011- 4027.
8. Matsuyama, K. et al. 1993. Termination mode and branching patterns of reticuloreticular and reticulospinal fibers of the nucleus reticularis pontis oralis in the cat: an anterograde PHA-L tracing study. Neurosci. Res. 17: 9-21.
9. Matsuyama, K. et al. 1999. Morphology of single pontine reticulospinal axons in the lumbar enlargement of the cat: a study using the anterograde tracer PHA-L. J. Comp. Neurol. 410: 413-430.
10. Davies, H.E. & S.A. Edgley . 1994. Inputs to group II-activated midlumbar interneurones from descending motor pathways in the cat. J. Physiol. 479: 463-473.
11. Jankowska, E. et al. 2005. Functional differentiation and organization of feline midlumbar commissural interneurones. J. Physiol. 565: 645-658.
12. Hammar, I., K. Stecina & E. Jankowska . 2007. Differential modulation by monoamine membrane receptor agonists of reticulospinal input to lamina VIII feline spinal commissural interneurons. Eur. J. Neurosci. 26: 1205-1212.
13. Jankowska, E. & K. Stecina . 2007. Uncrossed actions of feline corticospinal tract neurones on lumbar interneurones evoked via ipsilaterally descending pathways. J. Physiol. 580: 133-147.
14. O'Donovan, M.J. et al. 2005. Calcium imaging of network function in the developing spinal cord. Cell Calcium 37: 443-450.
15. Wilson, J.M. et al. 2007. Two-photon calcium imaging of network activity in XFP-expressing neurons in the mouse. J. Neurophysiol. 97: 3118-3125.
16. Vargas-Lizardi, P. & K.M. Lyser . 1974. Time of origin of Mauthner's neuron in Xenopus laevis embryos. Dev. Biol. 38: 220-228.
17. Mendelson, B. 1986. Development of reticulospinal neurons of the zebrafish. I: time of origin. J. Comp. Neurol. 251: 160-171.
18. Sechrist, J. & M. Bronner-Fraser . 1991. Birth and differentiation of reticular neurons in the chick hindbrain: ontogeny of the first neuronal population. Neuron 7: 947-963.
19. Pierce, E.T. 1973. Time of origin of neurons in the brain stem of the mouse. Prog. Brain Res. 40: 53-65.
20. McConnell, J.A. 1981. Identification of early neurons in the brainstem and spinal cord. II: an autoradiographic study in the mouse. J. Comp. Neurol. 200: 273-288.
21. Nornes, H.O. & M. Carry . 1978. Neurogenesis in spinal cord of mouse: an autoradiographic analysis. Brain Res. 159: 1-16.
22. Benito-Gonzalez, A. & F.J. Alvarez . 2012. Renshaw cells and Ia Inhibitory interneurons are generated at different times from p1 progenitors and differentiate shortly after exiting the cell cycle. J. Neurosci. 32: 1156-1170.
23. Glover, J.C., J.S. Renaud & F.M. Rijli . 2006. Retinoic acid and hindbrain patterning. J. Neurobiol 66: 705-725.
24. Auclair, F., R. Marchand & J.C. Glover . 1999. Regional patterning of reticulospinal and vestibulospinal neurons in the hindbrain of mouse and rat embryos. J. Comp. Neurol. 411: 288-300.
25. Pasqualetti, M. et al. 2007. Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J. Neurosci. 27: 9670-9681.
26. Chen, Y. et al. 2012. Hoxb1 controls anteroposterior identity of vestibular projection neurons. PLoS One 7: e34762.
27. VanderHorst, V.G. & B. Ulfhake . 2006. The organization of the brainstem and spinal cord of the mouse: relationships between monoaminergic, cholinergic, and spinal projection systems. J. Chem. Neuroanat. 31: 2-36.
28. Liang, H., G. Paxinos & C. Watson . 2011. Projections from the brain to the spinal cord in the mouse. Brain Struct. Funct. 215: 159-186.
29. Cepeda-Nieto, A.C., S.L. Pfaff & A. Varela-Echavarria . 2005. Homeodomain transcription factors in the development of subsets of hindbrain reticulospinal neurons. Mol. Cell Neurosci. 28: 30-41.
30. Sholomenko, G.N. & M.J. Odonovan . 1995. Development and characterization of pathways descending to the spinal-cord in the embryonic chick. J. Neurophysiol. 73: 1223-1233.
31. Glover, J.C. & G. Petursdottir . 1988. Pathway specificity of reticulospinal and vestibulospinal projections in the 11-day chicken embryo. J. Comp. Neurol. 270: 25-38, 60-21.
32. Lance-Jones, C. 1982. Motoneuron cell death in the developing lumbar spinal cord of the mouse. Brain Res. 256: 473-479.
33. Yamamoto, Y. & E. Christopher . 1999. Patterns of programmed cell death in populations of developing spinal motoneurons in chicken, mouse, and rat. Dev. Biol. 214: 60-71.
34. Okado, N. & R.W. Oppenheim . 1984. Cell death of motoneurons in the chick embryo spinal cord. IX. The loss of motoneurons following removal of afferent inputs. J. Neurosci. 4: 1639-1652.
35. Qin-Wei, Y. et al. 1994. Cell death of spinal motoneurons in the chick embryo following deafferentation: Rescue effects of tissue extracts, soluble proteins, and neurotrophic agents. J. Neurosci. 14: 7629-7640.
36. Borgius, L. et al. 2010. A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons. Mol. Cell Neurosci. 45: 245-257.
37. Hagglund, M. et al. 2010. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat. Neurosci. 13: 246-252.
38. Martin, E.M. et al. 2011. Molecular and neuroanatomical characterization of single neurons in the mouse medullary gigantocellular reticular nucleus. J. Comp. Neurol. 519: 2574-2593.
39. Szokol, K., J.C. Glover & M.-C. Perreault . 2008. Differential origin of reticulospinal drive to motoneurons innervating trunk and hindlimb muscles in the mouse revealed by optical recording. J. Physiol. 586: 5259-5276.
40. O'Donovan, M.J. et al. 1993. Real-time imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes. J. Neurosci. Methods 46: 91-106.
41. Lev-Tov, A. & M.J. O'Donovan . 1995. Calcium imaging of motoneuron activity in the en-bloc spinal cord preparation of the neonatal rat. J. Neurophysiol. 74: 1324-1334.
42. Kasumacic, N., J.C. Glover & M.-C. Perreault . 2010. Segmental patterns of vestibular-mediated synaptic inputs to axial and limb motoneurons in the neonatal mouse assessed by optical recording. J. Physiol. 588: 4905-4925.
43. Szokol, K. & M.-C. Perreault . 2009. Imaging synaptically mediated responses produced by brainstem inputs onto identified spinal neurons in the neonatal mouse. J. Neurosci. Methods 180: 1-8.
44. Galea, M.P. et al. 2010. Bilateral postsynaptic actions of pyramidal tract and reticulospinal neurons on feline erector spinae motoneurons. J. Neurosci. 30: 858-869.
45. Szokol, K., J.C. Glover & M.-C. Perreault . 2011. Organization of functional synaptic connections between medullary reticulospinal neurons and lumbar descending commissural interneurons in the neonatal mouse. J. Neurosci. 31: 4731- 4742.
46. Floeter, M.K. & A. Lev-Tov . 1993. Excitation of lumbar motoneurons by the medial longitudinal fasciculus in the in vitro brain stem spinal cord preparation of the neonatal rat. J. Neurophysiol. 70: 2241-2250.
47. Jankowska, E. 1992. Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38: 335-378.
48. Jankowska, E. & S.A. Edgley . 2010. Functional subdivision of feline spinal interneurons in reflex pathways from group Ib and II muscle afferents; an update. Eur. J. Neurosci. 32: 881-893.
49. Alaynick, W.A., T.M. Jessell & S.L. Pfaff . 2011. SnapShot: spinal cord development. Cell 146: 178.
50. Quinlan, K.A. & O. Kiehn . 2007. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci. 27: 6521- 6530.
51. Butt, S.J.B. & O. Kiehn . 2003. Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38: 953-963.
52. Matsuyama, K. et al. 2004. Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J. Comp. Neurol. 474: 546-561.
53. Perreault, M.-C. 2012. Focal release of caged glutamate onto neurons in the ventral spinal cord. In Cellular and Network Functions in the Spinal Cord Conference. L. Ziskind-Conhaim, Ed.: 32. Madison, Wisconsin.
54. Tuszynski, M.H. & O. Steward . 2012. Concepts and methods for the study of axonal regeneration in the CNS. Neuron 74: 777-791.
55. van den Brand, R. et al. 2012. Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 336: 1182-1185.
56. Oudega, M. & M.A. Perez . 2012. Corticospinal reorganization after spinal cord injury. J. Physiol. 590: 3647-3663.
57. Steeves, J.D. et al. 1994. Permissive and restrictive periods for brainstem-spinal regeneration in the chick. Prog. Brain Res. 103: 243-262.
58. ten Donkelaar, H. 2000. Development and regenerative capacity of descending supraspinal pathways in tetrapods: a comparative approach. Adv. Anat. Embryol. Cell Biol. 154: 1-145.
59. Alstermark, B. & J. Ogawa . 2004. In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons. J. Neurophysiol. 92: 1958-1962.
60. Fisher, K.M., B. Zaaimi & S.N. Baker . 2012. Reticular formation responses to magnetic brain stimulation of primary motor cortex. J. Physiol. 590: 4045-4060.
61. Jin, Y. et al. 2002. Transplants of fibroblasts genetically modified to express BDNF promote axonal regeneration from supraspinal neurons following chronic spinal cord injury. Exp. Neurol. 177: 265-275.
62. Ballermann, M. & K. Fouad . 2006. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur. J. Neurosci. 23: 1988-1996.
63. Lu, P. et al. 2012. Motor axonal regeneration after partial and complete spinal cord transection. J. Neurosci. 32: 8208-8218.
64. Blesch, A. & M.H. Tuszynski . 2008. Spinal cord injury: plasticity, regeneration and the challenge of translational drug development. Trends Neurosc. 32: 41-47.
65. Fenrich, K.K. et al. 2007. Axonal regeneration and development of de novo axons from distal dendrites of adult feline commissural interneurons after a proximal axotomy. J. Comp. Neurol. 502: 1079-1097.
66. Fenrich, K.K. & P.K. Rose . 2009. Spinal interneuron axons spontaneously regenerate after spinal cord injury in the adult feline. J. Neurosci. 29: 12145-12158.
67. Soteropoulos, D.S., S.A. Edgley & S.N. Baker . 2011. Lack of evidence for direct corticospinal contributions to control of the ipsilateral forelimb in monkey. J. Neurosci. 31: 11208-11219.
68. Baker, S.N. 2011. The primate reticulospinal tract, hand function and functional recovery. J. Physiol. 589: 5603-5612.
69. Riddle, C.N., S.A. Edgley & S.N. Baker . 2009. Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J. Neurosci. 29: 4993-4999.
70. Zaaimi, B. et al. 2012. Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135: 2277-2289.
71. Peterson, B.W. 1979. Reticulospinal projections to spinal motor nuclei. Annu. Rev. Physiol. 41: 127-140.
72. Drew, T. & S. Rossignol . 1990. Functional organization within the medullary reticular formation of intact unanesthetized cat. I: movements evoked by microstimulation. J. Neurophysiol. 64: 767-781.
73. Perreault, M.-C., T. Drew & S. Rossignol . 1993. Activity of medullary reticulospinal neurons during fictive locomotion. J. Neurphysiol. 69: 2232-2247.