Bilateral connectivity in the brainstem respiratory networks of lampreys

Journal of Comparative Neurology

Volumn 520, Issue 7, 2012, Pages 1442-1456

  Gariépy, Jean François ^a   Missaghi, Kianoush ^a   Chartré, Shannon ^b   Robert, Maxime ^b   Auclair, François ^a   Dubuc, Réjean ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Anterograde labeling; Bilateral; Descending command; Neuroanatomy; Respiration; Retrograde labeling; Whole cell patch recordings

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; LIDOCAINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN METABOLISM; BRAIN STEM; CELL LABELING; CELL POPULATION; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LAMPREY; MOTONEURON; NERVE CELL NETWORK; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RESPIRATION CONTROL; SYNAPSE; WHOLE CELL;

ANIMALS; BRAIN STEM; DIAPHRAGM; FUNCTIONAL LATERALITY; LAMPREYS; MOTOR NEURONS; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RESPIRATION;

EID: 84857925877     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22804     Document Type: Article

References (63)

1. Abdala AP, Rybak IA, Smith JC, Zoccal DB, Machado BH, St John WM, Paton JF. 2009. Multiple pontomedullary mechanisms of respiratory rhythmogenesis. Respir Physiol Neurobiol 168: 19-25.
2. Alheid GF, Gray PA, Jiang MC, Feldman JL, McCrimmon DR. 2002. Parvalbumin in respiratory neurons of the ventrolateral medulla of the adult rat. J Neurocytol 31: 693-717.
3. Arata A, Tanaka I, Fujii M, Ezure K. 2010. Active inspiratory-expiratory phase switching mechanism exists in the neonatal nucleus parabrachialis. Adv Exp Med Biol 669: 135-138.
4. Barnes BJ, Tuong CM, Mellen NM. 2007. Functional imaging reveals respiratory network activity during hypoxic and opioid challenge in the neonate rat tilted sagittal slab preparation. J Neurophysiol 97: 2283-2292.
5. Berger AJ. 2000. Determinants of respiratory motoneuron output. Respir Physiol 122: 259-269.
6. Bianchi AL, Pásaro R. 1997. Organization of central respiratory neurons. In: Miller AD, Bianchi AL, Bishop BP, editors. Neural control of the respiratory muscles. Boca Raton, FL: CRC Press.
7. Bouvier J, Thoby-Brisson M, Renier N, Dubreuil V, Ericson J, Champagnat J, Pierani A, Chédotal A, Fortin G. 2010. Hindbrain interneurons and axon guidance signaling critical for breathing. Nat Neurosci 13: 1066-1074.
8. Brocard F, Ryczko D, Fénelon K, Hatem R, Gonzales D, Auclair F, Dubuc R. 2010. The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J Neurosci 30: 523-533.
9. Cabelguen JM, Bourcier-Lucas C, Dubuc R. 2003. Bimodal locomotion elicited by electrical stimulation of the midbrain in the salamander Notophthalmus viridescens. J Neurosci 23: 2434-2439.
10. Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL. 1992. Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends Neurosci 15: 434-438.
11. Cohen MI. 1971. Switching of the respiratory phases and evoked phrenic responses produced by rostral pontine electrical stimulation. J Physiol 217: 133-158.
12. Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL. 2005. Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25: 446-453.
13. Del Negro CA, Pace RW, Hayes JA. 2008. What role do pacemakers play in the generation of respiratory rhythm? Adv Exp Med Biol 605: 88-93.
14. Dobbins EG, Feldman JL. 1994. Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 347: 64-86.
15. Dubuc R. 2009. Locomotor regions in the midbrain (MLR) and diencephalon (DLR). In: Binder MD, Hirokawa N, Windhorst U, editors. The encyclopedia of neuroscience. New York: Springer.
16. Duffin J, Li YM. 2006. Transmission of respiratory rhythm: midline-crossing connections at the level of the phrenic motor nucleus? Respir Physiol Neurobiol 153: 139-147.
17. Ellenberger HH, Feldman JL. 1988. Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J Comp Neurol 269: 47-57.
18. Ezure K, Tanaka I, Saito Y. 2003. Brainstem and spinal projections of augmenting expiratory neurons in the rat. Neurosci Res 45: 41-51.
19. Fagerstedt P, Zelenin PV, Deliagina TG, Orlovsky GN, Grillner S. 2000. Crossed reciprocal inhibition evoked by electrical stimulation of the lamprey spinal cord. Exp Brain Res 134: 147-154.
20. Feldman JL. 2010. Looking forward to breathing. Prog Brain Res 188: 213-218.
21. Feldman JL, Janczewski WA. 2006. Counterpoint: the preBötC is the primary site of respiratory rhythm generation in the mammal. J Appl Physiol 100: 2094-2098.
22. Feldman JL, Loewy AD, Speck DF. 1985. Projections from the ventral respiratory group to phrenic and intercostal motoneurons in cat: an autoradiographic study. J Neurosci 5: 1993-2000.
23. 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.
24. Glover JC, Petursdottir G, Jansen JK. 1986. Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. J Neurosci Methods 18: 243-254.
25. Goshgarian HG, Ellenberger HH, Feldman JL. 1991. Decussation of bulbospinal respiratory axons at the level of the phrenic nuclei in adult rats: a possible substrate for the crossed phrenic phenomenon. Exp Neurol 111: 135-139.
26. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL. 1999. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286: 1566-1568.
27. Gray PA, Hayes JA, Ling GY, Llona I, Tupal S, Picardo MC, Ross SE, Hirata T, Corbin JG, Eugenín J, Del Negro CA. 2010. Developmental origin of preBötzinger complex respiratory neurons. J Neurosci 30: 14883-14895.
28. Greer JJ, Smith JC, Feldman JL. 1991. Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437: 727-749.
29. Grillner S. 2003. The motor infrastructure: from ion channels to neural networks. Nat Rev Neurosci 4: 573-586.
30. Guimond JC, Auclair F, Lund JP, Dubuc R. 2003. Anatomical and physiological study of respiratory motor innervation in lampreys. Neuroscience 122: 259-266.
31. Hwang JC, Chien CT, St John WM. 1988. Characterization of respiratory-related activity of the facial nerve. Respir Physiol 73: 175-187.
32. Janczewski WA, Feldman JL. 2006. Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570: 407-420.
33. Janczewski WA, Karczewski WA. 1990. The role of neural connections crossed at the cervical level in determining rhythm and amplitude of respiration in cats and rabbits. Respir Physiol 79: 163-175.
34. Kawasaki R. 1979. Breathing rhythm-generation in the adult lamprey, Entosphenus japonicus. Jpn J Physiol 29: 327-338.
35. Kinkead R. 2009. Phylogenetic trends in respiratory rhythmogenesis: insights from ectothermic vertebrates. Respir Physiol Neurobiol 168: 39-48.
36. Koizumi H, Nomura K, Yokota Y, Enomoto A, Yamanishi T, Lida S, Ishihama K, Kogo M. 2009. Regulation of trigeminal respiratory motor activity in the brainstem. J Dent Res 88: 1048-1053.
37. Kozlov A, Huss M, Lansner A, Kotaleski JH, Grillner S. 2009. Simple cellular and network control principles govern complex patterns of motor behavior. Proc Natl Acad Sci U S A 106: 20027-20032.
38. Le Ray D, Juvin L, Ryczko D, Dubuc R. 2011. Supraspinal control of locomotion: the mesencephalic locomotor region. Prog Brain Res 188: 51-70.
39. Li YM, Shen L, Peever JH, Duffin J. 2003. Connections between respiratory neurones in the neonatal rat transverse medullary slice studied with cross-correlation. J Physiol 549: 327-332.
40. Martel B, Guimond JC, Gariépy J-F, Gravel J, Auclair F, Kolta A, Lund JP, Dubuc R. 2007. Respiratory rhythms generated in the lamprey rhombencephalon. Neuroscience 148: 279-293.
41. Martin E, Devidze N, Shelley D, Westberg L, Fontaine C, Pfaff D. 2011. Molecular and neuroanatomical characterization of single neurons in the mouse medullary gigantocellular reticular nucleus. J Comp Neurol 519: 2574-2593.
42. Matsushima T, Grillner S. 1992. Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J Neurophysiol 67: 373-388.
43. Mentel T, Cangiano L, Grillner S, Büschges A. 2008. Neural substrates for state-dependent changes in coordination between motoneuron pools during fictive locomotion in the lamprey spinal cord. J Neurosci 28: 868-879.
44. Mörschel M, Dutschmann M. 2009. Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philos Trans R Soc Lond B Biol Sci 364: 2517-2526.
45. Mutolo D, Bongianni F, Einum J, Dubuc R, Pantaleo T. 2007. Opioid-induced depression in the lamprey respiratory network. Neuroscience 150: 720-729.
46. Mutolo D, Bongianni F, Cinelli E, Pantaleo T. 2010. Role of neurokinin receptors and ionic mechanisms within the respiratory network of the lamprey. Neuroscience 169: 1136-1149.
47. Onimaru H, Homma I. 2003. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23: 1478-1486.
48. Onimaru H, Homma I. 2006. Point: the pFRG is the primary site of respiratory rhythm generation in the mammal. J Appl Physiol 100: 2094-2098.
49. Onimaru H, Kashiwagi M, Arata A, Homma I. 1993. Possible mutual excitatory couplings between inspiratory neurons in caudal ventrolateral medulla of brainstem-spinal cord preparation isolated from newborn rat. Neurosci Lett 150: 203-206.
50. Pace RW, Mackay DD, Feldman JL, Del Negro CA. 2007. Inspiratory bursts in the preBötzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J Physiol 582: 113-125.
51. Pagliardini S, Janczewski WA, Tan W, Dickson CT, Deisseroth K, Feldman JL. 2011. Active expiration induced by excitation of ventral medulla in adult anesthetized rats. J Neurosci 31: 2895-2905.
52. Rovainen CM. 1977. Neural control of ventilation in the lamprey. Fed Proc 36: 2386-2389.
53. Rubin JE, Hayes JA, Mendenhall JL, Del Negro CA. 2009. Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proc Natl Acad Sci U S A 106: 2939-2944.
54. Smith JC, Morrison DE, Ellenberger HH, Otto MR, Feldman JL. 1989. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 281: 69-96.
55. 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.
56. St. John WM. 2009. Noeud vital for breathing in the brainstem: gasping-yes, eupnoea-doubtful. Philos Trans R Soc Lond B Biol Sci 364: 2625-2633.
57. Tan W, Pagliardini S, Yang P, Janczewski WA, Feldman JL. 2010. Projections of preBötzinger complex neurons in adult rats. J Comp Neurol 518: 1862-1878.
58. Tarras-Wahlberg S, Rekling JC. 2009. Hypoglossal motoneurons in newborn mice receive respiratory drive from both sides of the medulla. Neuroscience 161: 259-268.
59. Thompson KJ. 1985. Organization of inputs to motoneurons during fictive respiration in the isolated lamprey brain. J Comp Physiol A 157: 291-302.
60. Vasilakos K, Wilson RJ, Kimura N, Remmers JE. 2005. Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats. J Neurobiol 62: 369-385.
61. von Euler C, Marttila I, Remmers JE, Trippenbach T. 1976. Effects of lesions in the parabrachial nucleus on the mechanisms for central and reflex termination of inspiration in the cat. Acta Physiol Scand 96: 324-337.
62. Wang J, Irnaten M, Venkatesan P, Evans C, Baxi S, Mendelowitz D. 2002. Synaptic activation of hypoglossal respiratory motorneurons during inspiration in rats. Acta Physiol Scand 3: 195-199.
63. Wilson RJ, Vasilakos K, Remmers JE. 2006. Phylogeny of vertebrate respiratory rhythm generators: the Oscillator Homology Hypothesis. Respir Physiol Neurobiol 154: 47-60.