Remote control of respiratory neural network by spinal locomotor generators

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Le Gal, Jean Patrick ^a   Juvin, Laurent ^a   Cardoit, Laura ^a   Thoby Brisson, Muriel ^a   Morin, Didier ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROKININ 1 RECEPTOR; N METHYLASPARTIC ACID; SEROTONIN;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN STEM; BREATHING RATE; CENTRAL PATTERN GENERATOR; CONTROLLED STUDY; IN VITRO STUDY; LOCOMOTION; MOTOR COORDINATION; NERVE CELL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROMODULATION; NEWBORN; NONHUMAN; PARAFACIAL RESPIRATORY GROUP; PHARMACOLOGICAL STIMULATION; PREINSPIRATORY NEURON; RAT; RESPIRATION CONTROL; RESPIRATORY NEURAL NETWORK; SPINAL CORD; ANIMAL; BREATHING; DRUG EFFECTS; ELECTROSTIMULATION; PHYSIOLOGY; RESPIRATION CENTER; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; ELECTRIC STIMULATION; LOCOMOTION; N-METHYLASPARTATE; NERVE NET; NEURONS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; RESPIRATION; RESPIRATORY CENTER; SEROTONIN; SPINAL CORD;

EID: 84897749402     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089670     Document Type: Article

References (81)

1. Mateika JH, Duffin J (1995) A review of the control of breathing during exercise. Eur J Appl Physiol Occup Physiol 71: 1-27.
2. Haouzi P, Hirsch JJ, Marchal F, Huszczuk A (1997) Ventilatory and gas exchange response during walking in severe peripheral vascular disease. Respir Physiol 107: 181-190. (Pubitemid 27173341)
3. Tobin MJ, Perez W, Guenther SM, D'Alonzo G, Dantzker DR (1986) Breathing pattern and metabolic behavior during anticipation of exercise. J Appl Physiol 60: 1306-1312. (Pubitemid 16028431)
4. Gravel J, Brocard F, Gariepy JF, Lund JP, Dubuc R (2007) Modulation of respiratory activity by locomotion in lampreys. Neuroscience 144: 1120-1132. (Pubitemid 46019840)
5. Bell HJ (2006) Respiratory control at exercise onset: an integrated systems perspective. Respir Physiol Neurobiol 152: 1-15.
6. Gariepy JF, Missaghi K, Dubuc R (2010) The interactions between locomotion and respiration. Prog Brain Res 187: 173-188.
7. Eldridge FL, Millhorn DE, Waldrop TG (1981) Exercise hyperpnea and locomotion: parallel activation from the hypothalamus. Science 211: 844-846. (Pubitemid 11132293)
8. Waldrop TG, Iwamoto GA (2006) Point: supraspinal locomotor centers do contribute significantly to the hyperpnea of dynamic exercise. J Appl Physiol 100: 1077-1079.
9. Gariepy JF, Missaghi K, Chevallier S, Chartre S, Robert M, et al. (2012) Specific neural substrate linking respiration to locomotion. Proc Natl Acad Sci U S A 109: E84-92.
10. Romaniuk JR, Kasicki S, Kazennikov OV, Selionov VA (1994) Respiratory responses to stimulation of spinal or medullary locomotor structures in decerebrate cats. Acta Neurobiol Exp (Wars) 54: 11-17. (Pubitemid 24113479)
11. Duysens J, Clarac F, Cruse H (2000) Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80: 83-133. (Pubitemid 30060562)
12. Pearson K (2000) Motor systems. Curr Opin Neurobiol 10: 649-654.
13. Iscoe S, Polosa C (1976) Synchronization of respiratory frequency by somatic afferent stimulation. J Appl Physiol 40: 138-148.
14. Kawahara K, Kumagai S, Nakazono Y, Miyamoto Y (1988) Analysis of entrainment of respiratory rhythm by somatic afferent stimulation in cats using phase response curves. Biol Cybern 58: 235-242. (Pubitemid 18070278)
15. Funk GD, Milsom WK, Steeves JD (1992) Coordination of wingbeat and respiration in the Canada goose. I. Passive wing flapping. J Appl Physiol 73: 1014-1024.
16. Morin D, Viala D (2002) Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs. J Neurosci 22: 4756-4765. (Pubitemid 37465691)
17. Potts JT, Rybak IA, Paton JF (2005) Respiratory rhythm entrainment by somatic afferent stimulation. J Neurosci 25: 1965-1978. (Pubitemid 40289401)
18. Giraudin A, Le Bon-Jego M, Cabirol MJ, Simmers J, Morin D (2012) Spinal and pontine relay pathways mediating respiratory rhythm entrainment by limb proprioceptive inputs in the neonatal rat. J Neurosci 32: 11841-11853.
19. Boggs DF (2002) Interactions between locomotion and ventilation in tetrapods. Comp Biochem Physiol A Mol Integr Physiol 133: 269-288.
20. Smith JC, Feldman JL (1987) In vitro brainstem-spinal cord preparations for study of motor systems for mammalian respiration and locomotion. J Neurosci Methods 21: 321-333. (Pubitemid 17141521)
21. Hayes HB, Chang YH, Hochman S (2009) An in vitro spinal cord-hindlimb preparation for studying behaviorally relevant rat locomotor function. J Neurophysiol 101: 1114-1122.
22. Hagglund 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. Antri M, Mellen N, Cazalets JR (2011) Functional organization of locomotor interneurons in the ventral lumbar spinal cord of the newborn rat. PLoS One 6: e20529.
24. Juvin L, Le Gal JP, Simmers J, Morin D (2012) Cervicolumbar coordination in mammalian quadrupedal locomotion: role of spinal thoracic circuitry and limb sensory inputs. J Neurosci 32: 953-965.
25. Ruangkittisakul A, Secchia L, Bornes TD, Palathinkal DM, Ballanyi K (2007) Dependence on extracellular Ca2+/K+ antagonism of inspiratory centre rhythms in slices and en bloc preparations of newborn rat brainstem. J Physiol 584: 489-508. (Pubitemid 47578334)
26. Panaitescu B, Ruangkittisakul A, Ballanyi K (2010) Depression by Ca2+ and stimulation by K+ of fictive inspiratory rhythm in newborn rat brainstem slices. Adv Exp Med Biol 669: 91-95.
27. Richards CD, Sercombe R (1970) Calcium, magnesium and the electrical activity of guinea-pig olfactory coex in vitro. J Physiol 211: 571-584.
28. Telgkamp P, Cao YQ, Basbaum AI, Ramirez JM (2002) Long-term deprivation of substance P in PPT-A mutant mice alters the anoxic response of the isolated respiratory network. J Neurophysiol 88: 206-213. (Pubitemid 34755344)
29. Janczewski WA, Onimaru H, Homma I, Feldman JL (2002) Opioid-resistant respiratory pathway from the preinspiratory neurones to abdominal muscles: in vivo and in vitro study in the newborn rat. J Physiol 545: 1017-1026. (Pubitemid 36024437)
30. Giraudin A, Cabirol-Pol MJ, Simmers J, Morin D (2008) Intercostal and abdominal respiratory motoneurons in the neonatal rat spinal cord: spatiotemporal organization and responses to limb afferent stimulation. J Neurophysiol 99: 2626-2640.
31. Lev-Tov A, Delvolve I, Kremer E (2000) Sacrocaudal afferents induce rhythmic efferent bursting in isolated spinal cords of neonatal rats. J Neurophysiol 83: 888-894. (Pubitemid 30091298)
32. Whelan P, Bonnot A, O'Donovan MJ (2000) Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84: 2821-2833.
33. Etlin A, Finkel E, Mor Y, O'Donovan MJ, Anglister L, et al. (2013) Characterization of sacral interneurons that mediate activation of locomotor pattern generators by sacrocaudal afferent input. J Neurosci 33: 734-747.
34. Juvin L, Simmers J, Morin D (2005) Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 25: 6025-6035. (Pubitemid 40911434)
35. Mellen NM, Thoby-Brisson M (2012) Respiratory circuits: development, function and models. Curr Opin Neurobiol 22: 676-685.
36. Onimaru H, Homma I (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23: 1478-1486. (Pubitemid 36258926)
37. Onimaru H, Homma I (1992) Whole cell recordings from respiratory neurons in the medulla of brainstem-spinal cord preparations isolated from newborn rats. Pflugers Arch 420: 399-406.
38. Thoby-Brisson M, Karlen M, Wu N, Charnay P, Champagnat J, et al. (2009) Genetic identification of an embryonic parafacial oscillator coupling to the preBotzinger complex. Nat Neurosci 12: 1028-1035.
39. Mulkey DK, Rosin DL, West G, Takakura AC, Moreira TS, et al. (2007) Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pH-independent mechanism. J Neurosci 27: 14128-14138. (Pubitemid 351377869)
40. Onimaru H, Ikeda K, Kawakami K (2008) CO2-sensitive preinspiratory neurons of the parafacial respiratory group express Phox2b in the neonatal rat. J Neurosci 28: 12845-12850.
41. Onimaru H, Ikeda K, Kawakami K (2009) Phox2b, RTN/pFRG neurons and respiratory rhythmogenesis. Respir Physiol Neurobiol 168: 13-18.
42. Guyenet PG, Mulkey DK (2010) Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol 173: 244-255.
43. Armstrong DM (1988) The supraspinal control of mammalian locomotion. J Physiol 405: 1-37.
44. Jordan LM (1998) Initiation of locomotion in mammals. Ann N Y Acad Sci 860: 83-93.
45. Matsuyama K, Drew T (2000) Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. I. Walking on a level surface. J Neurophysiol 84: 2237-2256.
46. Arshavsky YI, Berkinblit MB, Fukson OI, Gelfand IM, Orlovsky GN (1972) Origin of modulation in neurones of the ventral spinocerebellar tract during locomotion. Brain Res 43: 276-279.
47. Buchanan JT, Einum JF (2008) The spinobulbar system in lamprey. Brain Res Rev 57: 37-45. (Pubitemid 350213102)
48. Fedirchuk B, Stecina K, Kristensen KK, Zhang M, Meehan CF, et al. (2013) Rhythmic activity of feline dorsal and ventral spinocerebellar tract neurons during fictive motor actions. J Neurophysiol 109: 375-388.
49. Dubuc R, Grillner S (1989) The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 96: 196-200. (Pubitemid 19082459)
50. Antri M, Fenelon K, Dubuc R (2009) The contribution of synaptic inputs to sustained depolarizations in reticulospinal neurons. J Neurosci 29: 1140-1151.
51. Buchanan JT (2011) Spinal locomotor inputs to individually identified reticulospinal neurons in the lamprey. J Neurophysiol 106: 2346-2357.
52. Bussieres N, Dubuc R (1992) Phasic modulation of vestibulospinal neuron activity during fictive locomotion in lampreys. Brain Res 134: 174-179.
53. Beyeler A, Metais C, Combes D, Simmers J, Le Ray D (2008) Metamorphosis-induced changes in the coupling of spinal thoraco-lumbar motor outputs during swimming in Xenopus laevis. J Neurophysiol 100: 1372-1383.
54. Falgairolle M, Cazalets JR (2007) Metachronal coupling between spinal neuronal networks during locomotor activity in newborn rat. J Physiol 580: 87-102. (Pubitemid 46470646)
55. Combes D, Le Ray D, Lambert FM, Simmers J, Straka H (2008) An intrinsic feed-forward mechanism for vertebrate gaze stabilization. Curr Biol 18: R241-243. (Pubitemid 351392069)
56. Lambert FM, Combes D, Simmers J, Straka H (2012) Gaze stabilization by efference copy signaling without sensory feedback during vertebrate locomotion. Curr Biol 22: 1649-1658.
57. von Uckermann G, Le Ray D, Combes D, Straka H, Simmers J (2013) Spinal efference copy signaling and gaze stabilization during locomotion in juvenile Xenopus frogs. J Neurosci 33: 4253-4264.
58. Janczewski WA, Feldman JL (2006) Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570: 407-420.
59. Wittmeier S, Song G, Duffin J, Poon CS (2008) Pacemakers handshake synchronization mechanism of mammalian respiratory rhythmogenesis. Proc Natl Acad Sci U S A 105: 18000-18005.
60. Pagliardini S, Janczewski WA, Tan W, Dickson CT, Deisseroth K, et al. (2011) Active expiration induced by excitation of ventral medulla in adult anesthetized rats. J Neurosci 31: 2895-2905.
61. Feldman JL, Del Negro CA, Gray PA (2013) Understanding the rhythm of breathing: so near, yet so far. Annu Rev Physiol 75: 423-452.
62. Guyenet PG, Mulkey DK, Stornetta RL, Bayliss DA (2005) Regulation of ventral surface chemoreceptors by the central respiratory pattern generator. J Neurosci 25: 8938-8947. (Pubitemid 41384462)
63. Voituron N, Frugiere A, Champagnat J, Bodineau L (2006) Hypoxia-sensing properties of the newborn rat ventral medullary surface in vitro. J Physiol 577: 55-68. (Pubitemid 44698240)
64. Ballanyi K, Ruangkittisakul A, Onimaru H (2009) Opioids prolong and anoxia shortens delay between onset of preinspiratory (pFRG) and inspiratory (preBotC) network bursting in newborn rat brainstems. Pflugers Arch 458: 571-587.
65. Dubreuil V, Thoby-Brisson M, Rallu M, Persson K, Pattyn A, et al. (2009) Defective respiratory rhythmogenesis and loss of central chemosensitivity in Phox2b mutants targeting retrotrapezoid nucleus neurons. J Neurosci 29: 14836-14846.
66. Gestreau C, Heitzmann D, Thomas J, Dubreuil V, Bandulik S, et al. (2010) Task2 potassium channels set central respiratory CO2 and O2 sensitivity. Proc Natl Acad Sci U S A 107: 2325-2330.
67. Onimaru H, Ikeda K, Kawakami K (2012) Postsynaptic mechanisms of CO(2) responses in parafacial respiratory neurons of newborn rats. J Physiol 590: 1615-1624.
68. Wang S, Shi Y, Shu S, Guyenet PG, Bayliss DA (2013) Phox2b-expressing retrotrapezoid neurons are intrinsically responsive to H+ and CO2. J Neurosci 33: 7756-7761.
69. Tan W, Pagliardini S, Yang P, Janczewski WA, Feldman JL (2010) Projections of preBotzinger complex neurons in adult rats. J Comp Neurol 518: 1862-1878.
70. Bochorishvili G, Stornetta RL, Coates MB, Guyenet PG (2012) Pre-Botzinger complex receives glutamatergic innervation from galaninergic and other retrotrapezoid nucleus neurons. J Comp Neurol 520: 1047-1061.
71. Voituron N, Shvarev Y, Menuet C, Bevengut M, Fasano C, et al. (2010) Fluoxetine treatment abolishes the in vitro respiratory response to acidosis in neonatal mice. PLoS One 5: e13644.
72. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL (1991) Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729.
73. Rudzinski E, Kapur RP (2010) PHOX2B immunolocalization of the candidate human retrotrapezoid nucleus. Pediatr Dev Pathol 13: 291-299.
74. Shvarev YN, Lagercrantz H, Yamamoto Y (2002) Biphasic effects of substance P on respiratory activity and respiration-related neurones in ventrolateral medulla in the neonatal rat brainstem in vitro. Acta Physiol Scand 174: 67-84. (Pubitemid 34122102)
75. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL (1999) Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex. Science 286: 1566-1568.
76. Gray PA, Janczewski WA, Mellen N, McCrimmon DR, Feldman JL (2001) Normal breathing requires preBotzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 4: 927-930. (Pubitemid 32801596)
77. Guyenet PG, Wang H (2001) Pre-Botzinger neurons with preinspiratory discharges "in vivo" express NK1 receptors in the rat. J Neurophysiol 86: 438-446. (Pubitemid 32623247)
78. Stornetta RL, Rosin DL, Wang H, Sevigny CP, Weston MC, et al. (2003) A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Botzinger complex. J Comp Neurol 455: 499-512. (Pubitemid 36043652)
79. Ben-Mabrouk F, Tryba AK (2010) Substance P modulation of TRPC3/7 channels improves respiratory rhythm regularity and ICAN-dependent pacemaker activity. Eur J Neurosci 31: 1219-1232.
80. Hayes JA, Del Negro CA (2007) Neurokinin receptor-expressing pre-botzinger complex neurons in neonatal mice studied in vitro. J Neurophysiol 97: 4215-4224. (Pubitemid 47080652)
81. Johnson SM, Smith JC, Feldman JL (1996) Modulation of respiratory rhythm in vitro: role of Gi/o protein-mediated mechanisms. J Appl Physiol 80: 2120-2133. (Pubitemid 26243793)