Organization of functional synaptic connections between medullary reticulospinal neurons and lumbar descending commissural interneurons in the neonatal mouse

Journal of Neuroscience

Volumn 31, Issue 12, 2011, Pages 4731-4742

  Szokol, Karolina ^a   Glover, Joel C ^a   Perreault, Marie Claude ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MEPHENESIN; CENTRAL MUSCLE RELAXANT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; BRAIN REGION; CELL POPULATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HINDLIMB; INTERNEURON; LUMBAR SPINAL CORD; MOUSE; NERVE CELL STIMULATION; NEUROMUSCULAR FUNCTION; NEWBORN; NONHUMAN; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; RETICULOSPINAL TRACT; SKELETAL MUSCLE; SPINAL CORD MOTONEURON; SYNAPTIC TRANSMISSION; ANIMAL; CALCIUM SIGNALING; CYTOLOGY; DRUG EFFECTS; ELECTROSTIMULATION; EVOKED RESPONSE; FLUORESCENCE MICROSCOPY; HEMISPHERIC DOMINANCE; IN VITRO STUDY; INSTITUTE FOR CANCER RESEARCH MOUSE; MEDULLA OBLONGATA; NERVE CELL; NERVE FIBER; PHYSIOLOGY; RETICULAR FORMATION; SPINAL CORD;

ANIMALS; ANIMALS, NEWBORN; AXONS; CALCIUM SIGNALING; ELECTRIC STIMULATION; EVOKED POTENTIALS; FUNCTIONAL LATERALITY; INTERNEURONS; MEDULLA OBLONGATA; MEPHENESIN; MICE; MICE, INBRED ICR; MICROSCOPY, FLUORESCENCE; MUSCLE RELAXANTS, CENTRAL; NEURONS; RETICULAR FORMATION; SPINAL CORD; SYNAPTIC TRANSMISSION; IN VITRO TECHNIQUES;

EID: 79953023025     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5486-10.2011     Document Type: Article

References (66)

1. Al-Mosawie A, Wilson JM, Brownstone RM (2007) Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. Eur J Neurosci 26:3003-3015. (Pubitemid 350135168)
2. Alstermark B, Ogawa J (2004) In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons. J Neurophysiol 92:1958-1962.
3. Alstermark B, Ogawa J, Isa T (2004) Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol 91:1832-1839. (Pubitemid 38339351)
4. Brownstone RM, Wilson JM (2008) Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 57:64-76. (Pubitemid 350213100)
5. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953-963. (Pubitemid 36782385)
6. Butt SJ, Harris-Warrick RM, Kiehn O (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22:9961-9971. (Pubitemid 35332881)
7. Cazalets JR, Borde M, Clarac F (1995) Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat. J Neurosci 15:4943-4951.
8. Cowley KC, Zaporozhets E, Joundi RA, Schmidt BJ (2009) Contribution of commissural projections to bulbospinal activation of locomotion in the in vitro neonatal rat spinal cord. J Neurophysiol 101:1171-1178.
9. Deliagina TG, Orlovsky GN, Zelenin PV, Beloozerova IN (2006) Neural bases of postural control. Physiology 21:216-225. (Pubitemid 43801251)
10. Díaz-Ríos M, Dombeck DA, Webb WW, Harris-Warrick RM (2007) Serotonin modulates dendritic calcium influx in commissural interneurons in the mouse spinal locomotor network. J Neurophysiol 98:2157-2167. (Pubitemid 47584401)
11. Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251-261. (Pubitemid 37443000)
12. Eide AL, Glover J, Kjaerulff O, Kiehn O (1999) Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord. J Comp Neurol 403:332-345. (Pubitemid 29006216)
13. Floeter MK, Lev-Tov A (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. (Pubitemid 24006821)
14. Floeter MK, Sholomenko GN, Gossard JP, Burke RE (1993) Disynaptic excitation from the medial longitudinal fasciculus to lumbosacral motoneurons: modulation by repetitive activation, descending pathways, and locomotion. Exp Brain Res 92:407-419. (Pubitemid 23068677)
15. Garcia-Rill E, Homma Y, Skinner RD (2004) Arousal mechanisms related to posture and locomotion. I. Descending modulation. Prog Brain Res 143:283-290. (Pubitemid 37443002)
16. Glover JC (1995) Retrograde and anterograde axonal tracing with fluorescent dextrans in the embryonic nervous system. Neurosci Protocols 30:1-13.
17. Gordon IT, Whelan PJ (2008) Brainstem modulation of locomotion in the neonatal mouse spinal cord. J Physiol 586:2487-2497. (Pubitemid 351689807)
18. Grillner S, Lund S (1968) The origin of a descending pathway with monosynaptic action on flexor motoneurones. Acta Physiol Scand 74:274-284.
19. Grillner S, Hongo T, Lund S (1968) Reciprocal effects between two descending bulbospinal systems with monosynaptic connections to spinal motoneurones. Brain Res 10:477-480.
20. Grillner S, Deliagina T, Ekeberg O, el Manira A, Hill RH, Lansner A, Orlovsky GN, Wallén P (1995) Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci 18:270-279.
21. Habaguchi T, Takakusaki K, Saitoh K, Sugimoto J, Sakamoto T (2002) Medullary reticulospinal tract mediating the generalized motor inhibition in cats. II. Functional organization within the medullary reticular formation with respect to postsynaptic inhibition of forelimb and hindlimb motoneurons. Neuroscience 113:65-77.
22. Hägglund M, Borgius L, Dougherty KJ, Kiehn O (2010) Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 13:246-252.
23. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L (2005) Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93:1439-1449. (Pubitemid 40283732)
24. Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38:335-378.
25. Jankowska E (2008) Spinal interneuronal networks in the cat: elementary components. Brain Res Rev 57:46-55.
26. Jankowska E, Edgley SA (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.
27. Jankowska E, Hammar I, Slawinska U, Maleszak K, Edgley SA (2003) Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. J Neurosci 23:1867-1878. (Pubitemid 36314742)
28. Jankowska E, Edgley SA, Krutki P, Hammar I (2005) Functional differentiation and organization of feline midlumbar commissural interneurones. J Physiol 565:645-658. (Pubitemid 40872489)
29. Jankowska E, Stecina K, Cabaj A, Pettersson LG, Edgley SA (2006) Neuronal relays in double crossed pathways between feline motor cortex and ipsilateral hindlimb motoneurones. J Physiol 575:527-541. (Pubitemid 44270179)
30. Jankowska E, Bannatyne BA, Stecina K, Hammar I, Cabaj A, Maxwell DJ (2009) Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: neurotransmitters, projections and target cells. J Physiol 587:401-418.
31. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG (2008) Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57:183-191. (Pubitemid 350213101)
32. Juvin L, Morin D (2005) Descending respiratory polysynaptic inputs to cervical and thoracic motoneurons diminish during early postnatal maturation in rat spinal cord. Eur J Neurosci 21:808-813. (Pubitemid 40363516)
33. Kasumacic N, Glover JC, Perreault MC (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.
34. Kiehn O, Quinlan KA, Restrepo CE, Lundfald L, Borgius L, Talpalar AE, Endo T (2008) Excitatory components of the mammalian locomotor CPG. Brain Res Rev 57:56-63. (Pubitemid 350213090)
35. Kjaerulff O, Kiehn O (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16:5777-5794. (Pubitemid 26293400)
36. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M (2004) Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42:375-386. (Pubitemid 38610137)
37. Lev-Tov A, Pinco M (1992) In vitro studies of prolonged synaptic depression in the neonatal rat spinal cord. J Physiol 447:149-169.
38. Li Y, Burke RE (2001) Short-term synaptic depression in the neonatal mouse spinal cord: effects of calcium and temperature. J Neurophysiol 85:2047-2062. (Pubitemid 32440683)
39. Lundfald L, Restrepo CE, Butt SJ, Peng CY, Droho S, Endo T, Zeilhofer HU, Sharma K, Kiehn O (2007) Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur J Neurosci 26:2989-3002. (Pubitemid 350135167)
40. Matsuyama K, Kobayashi Y, Takakusaki K, Mori S, Kimura H (1993) Termination mode and branching patterns of reticuloreticular and reticulospinal fibres of the nucleus reticularis pontis oralis in the cat: an anterograde PHA-L tracing study. Neurosci Res 17:9-21. (Pubitemid 23239265)
41. Matsuyama K, Takakusaki K, Nakajima K, Mori S (1997) Multi-segmental innervation of single pontine reticulospinal axons in the cervico-thoracic region of the cat: anterograde PHA-L tracing study. J Comp Neurol 377:234-250. (Pubitemid 27009831)
42. Matsuyama K, Mori F, Nakajima K, Drew T, Aoki M, Mori S (2004a) Locomotor role of the corticoreticular-reticulospinal-spinal interneuronal system. Prog Brain Res 143:239-249. (Pubitemid 37442999)
43. Matsuyama K, Nakajima K, Mori F, Aoki M, Mori S (2004b) Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J Comp Neurol 474:546-561. (Pubitemid 38720424)
44. Moran-Rivard L, Kagawa T, Saueressig H, Gross MK, Burrill J, Goulding M (2001) Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29:385-399. (Pubitemid 32206478)
45. Mori S, Iwakiri H, Homma Y, Yokoyama T, Matsuyama K (1995) Neuroanatomical and neurophysiological bases of postural control. Adv Neurol 67:289-303.
46. Nissen UV, Mochida H, Glover JC (2005) Development of projection-specific interneurons and projection neurons in the embryonic mouse and rat spinal cord. J Comp Neurol 483:30-47. (Pubitemid 40170685)
47. Paxinos G, Halliday G, Watson C, Koutcherov Y, Wang H (2007) Atlas of the developing mouse brain. London: Elsevier.
48. Perreault MC, Kasumacic N, Glover JC, Szokol K (2009) Bulbospinal control of lumbar motor networks in the neonatal mouse. Paper presented at Groupe de recherche sur le système nerveux central, Montreal, May.
49. Peterson BW (1979) Reticulospinal projections to spinal motor nuclei. Annu Rev Physiol 41:127-140.
50. Peterson BW, Maunz RA, Pitts NG, Mackel RG (1975) Patterns of projection and braching of reticulospinal neurons. Exp Brain Res 23:333-351.
51. Peterson BW, Pitts NG, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36:1-20. (Pubitemid 9215698)
52. Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, Jessell TM (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29:367-384. (Pubitemid 32206477)
53. Restrepo CE, Lundfald L, Szabó G, Erdélyi F, Zeilhofer HU, Glover JC, Kiehn O (2009) Transmitter-phenotypes of commissural interneurons in the lumbar spinal cord of newborn mice. J Comp Neurol 517:177-192.
54. Riddle CN, Edgley SA, Baker SN (2009) Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 29:4993-4999.
55. Sasaki S (1997) Axonal branching and termination of cervical reticulospinal neurons in the cat brachial segments. Neurosci Lett 228:83-86.
56. Sasaki S (1999) Direct connection of the nucleus reticularis gigantocellularis neurons with neck motoneurons in cats. Exp Brain Res 128:527-530.
57. Sasaki S, Yoshimura K, Naito K (2004) The neural control of orienting: role of multiple-branching reticulospinal neurons. Prog Brain Res 143:383-389. (Pubitemid 37443011)
58. Shapovalov AI (1969) Posttetanic potentiation of monosynaptic and disynaptic actions from supraspinal structures on lumbar motoneurons. J Neurophysiol 32:948-959.
59. Stokke MF, Nissen UV, Glover JC, Kiehn O (2002) Projection patterns of commissural interneurons in the lumbar spinal cord of the neonatal rat. J Comp Neurol 446:349-359. (Pubitemid 34303733)
60. Szokol K, Perreault MC (2009) Imaging synaptically mediated responses produced by brainstem inputs onto identified spinal neurons in the neonatal mouse. J Neurosci Methods 180:1-8.
61. Szokol K, Glover JC, Perreault MC (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.
62. Szokol K, Glover JC, Perreault MC (2009) Functional organization of reticulospinal inputs to lumbar commissural interneurons. Paper presented at SCRS, Madison, Wisconsin.
63. Vinay L, Cazalets JR, Clarac F (1995) Evidence for the existence of a functional polysynaptic pathway from trigeminal afferents to lumbar motoneurons in the neonatal rat. Eur J Neurosci 7:143-151.
64. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710-5719. (Pubitemid 40847883)
65. Wilson VJ, Yoshida M (1969) Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. J Neurophysiol 32:743-758.
66. Zhang Y, Narayan S, Geiman E, Lanuza GM, Velasquez T, Shanks B, Akay T, Dyck J, Pearson K, Gosgnach S, Fan CM, Goulding M (2008) V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60:84-96.