Peripheral oxygen-sensing cells directly modulate the output of an identified respiratory central pattern generating neuron

European Journal of Neuroscience

Volumn 25, Issue 12, 2007, Pages 3537-3550

  Bell, Harold J ^a   Inoue, Takuya ^a   Shum, Kelly ^a   Luk, Collin ^a   Syed, Naweed I ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Chemosensory neurons; Identified neurons; In vitro; In vivo; Lymnaea; Respiration

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREATHING; CELL FUNCTION; CELL ISOLATION; CHEMORECEPTOR; CHEMOSENSITIVITY; HYPOXIA; LYMNAEA; MEMBRANE DEPOLARIZATION; MOLLUSC; NERVE CELL; NERVE CELL CULTURE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; RESPIRATION CENTER; STATISTICAL SIGNIFICANCE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ANOXIA; ANTINEMATODAL AGENTS; BEHAVIOR, ANIMAL; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; GANGLIA, INVERTEBRATE; MAGNESIUM; MECAMYLAMINE; NERVE NET; NEURONS; NICOTINIC ANTAGONISTS; OXYGEN; RESPIRATION; SNAILS; SURAMIN; SYNAPTIC TRANSMISSION;

EID: 34347404903     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05607.x     Document Type: Article

References (61)

1. Benjamin, P.R. (1971) On the structure of the pulmonate osphradium. I. Cell types and their organisation. Z. Zellforsch. Mikrosk. Anat., 117, 485 501.
2. Dickinson, P.S. (2006) Neuromodulation of central pattern generators in invertebrates and vertebrates. Curr. Opin. Neurobiol., 16, 604 614.
3. Duffin, J. (2004) Functional organization of respiratory neurones: a brief review of current questions and speculations. Exp. Physiol., 89, 517 529.
4. Ezure, K. (2004) Reflections on respiratory rhythm generation. Prog. Brain Res., 143, 67 74.
5. Feldman, J.L. Del Negro, C.A. (2006) Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci., 7, 232 242.
6. Feldman, J.L. Janczewski, W.A. (2006) Point: Counterpoint: The parafacial respiratory group (pFRG)/pre-Botzinger complex (preBotC) is the primary site of respiratory rhythm generation in the mammal. Counterpoint: the preBotC is the primary site of respiratory rhythm generation in the mammal. J. Appl. Physiol., 100, 2096 2097 Discussion, 2097-2099, 2103-2098.
7. Feldman, J.L., Mitchell, G.S. Nattie, E.E. (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci., 26, 239 266.
8. Feng, Z.P., Klumperman, J., Lukowiak, K. Syed, N.I. (1997) In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. J. Neurosci., 17, 7839 7849.
9. Feng, Z.P., Hasan, S.U., Lukowiak, K. Syed, N.I. (2000) Target cell contact suppresses neurite outgrowth from soma-soma paired Lymnaea neurons. J. Neurobiol., 42, 357 369.
10. Feng, Z.P., Grigoriev, N., Munno, D., Lukowiak, K., MacVicar, B.A., Goldberg, J.I. Syed, N.I. (2002) Development of Ca2+ hotspots between Lymnaea neurons during synaptogenesis. J. Physiol., 539, 53 65.
11. Gilmour, K.M. (2001) The CO2/pH ventilatory drive in fish. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 130, 219 240.
12. Gourine, A.V. (2005) On the peripheral and central chemoreception and control of breathing: an emerging role of ATP. J. Physiol., 568, 715 724.
13. Hamakawa, T., Woodin, M.A., Bjorgum, M.C., Painter, S.D., Takasaki, M., Lukowiak, K., Nagle, G.T. Syed, N.I. (1999) Excitatory synaptogenesis between identified Lymnaea neurons requires extrinsic trophic factors and is mediated by receptor tyrosine kinases. J. Neurosci., 19, 9306 9312.
14. Haque, Z., Lee, T.K., Inoue, T., Luk, C., Hasan, S.U., Lukowiak, K. Syed, N.I. (2006) An identified central pattern-generating neuron co-ordinates sensory-motor components of respiratory behavior in Lymnaea. Eur. J. Neurosci., 23, 94 104.
15. Honda, Y. (1985) Role of carotid chemoreceptors in control of breathing at rest and in exercise: studies on human subjects with bilateral carotid body resection. Jpn J. Physiol., 35, 535 544.
16. Inoue, T., Haque, Z., Lukowiak, K. Syed, N.I. (2001) Hypoxia-induced respiratory patterned activity in Lymnaea originates at the periphery. J. Neurophysiol., 86, 156 163.
17. Jones, J.D. (1961) Aspects of respiration in Planorbis corneus L. & Lymnaea stagnalis L. (gastropoda: pulmonata). Comp. Biochem. Physiol., 4, 1 29.
18. Kamardin, N.N. (1976a) Reactions of the osphradium of the mollusk Lymnea stagnalis to different concentrations of oxygen in water. Zh. Evol. Biokhim. Fiziol., 12, 481 482.
19. Kamardin, N.N. (1976b) Structure and cellular organization of the osphradium of Lymnaea stagnalis L. Arkh. Anat. Gistol. Embriol., 71, 87 90.
20. Kamardin, N., Szucs, A. Rozsa, K.S. (1999) Distinct responses of osphradial neurons to chemical stimuli and neurotransmitters in Lymnaea stagnalis L. Cell Mol. Neurobiol., 19, 235 247.
21. Kamardin, N.N., Shalanki, Y., Rozha, K.S. Nozdrachev, A.D. (2001) Studies of chemoreceptor perception in mollusks. Neurosci. Behav. Physiol., 31, 227 235.
22. Kubin, L., Alheid, G.F., Zuperku, E.J. McCrimmon, D.R. (2006) Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol., 101, 618 627.
23. Kusakabe, T. (2002) Carotid labyrinth of amphibians. Microsc. Res. Tech., 59, 207 226.
24. Lahiri, S. Forster, R.E. 2nd (2003) CO2/H(+) sensing: peripheral and central chemoreception. Int. J. Biochem. Cell Biol., 35, 1413 1435.
25. Lieske, S.P., Thoby-Brisson, M., Telgkamp, P. Ramirez, J.M. (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat. Neurosci., 3, 600 607.
26. Lukowiak, K., Ringseis, E., Spencer, G., Wildering, W. Syed, N. (1996) Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. J. Exp. Biol., 199, 683 691.
27. Lukowiak, K., Martens, K., Orr, M., Parvez, K., Rosenegger, D. Sangha, S. (2006) Modulation of aerial respiratory behaviour in a pond snail. Resp. Physiol. Neurobiol., 154, 61 72.
28. Magoski, N.S., Syed, N.I. Bulloch, A.G. (1994) A neuronal network from the mollusc Lymnaea stagnalis. Brain Res., 645, 201 214.
29. Milsom, W.K. (1995) The role of CO2/pH chemoreceptors in ventilatory control. Braz. J. Med. Biol. Res., 28, 1147 1160.
30. Miserocchi, G. (1976) Role of peripheral and central chemosensitive afferents in the control of depth and frequency of breathing. Resp. Physiol., 26, 101 111.
31. Mitchell, G.S., Baker, T.L., Nanda, S.A., Fuller, D.D., Zabka, A.G., Hodgeman, B.A., Bavis, R.W., Mack, K.J. Olson, E.B. Jr. (2001) Invited review: Intermittent hypoxia and respiratory plasticity. J. Appl. Physiol., 90, 2466 2475.
32. Nezlin, L.P. (1995) Primary sensory neurons and their central projections in the pond snail Lymnaea stagnalis. Acta Biol. Hung., 46, 305 313.
33. Nurse, C.A. (2005) Neurotransmission and neuromodulation in the chemosensory carotid body. Auton. Neurosci., 120, 1 9.
34. Olson, E.B. Jr., Vidruk, E.H. Dempsey, J.A. (1988) Carotid body excision significantly changes ventilatory control in awake rats. J. Appl. Physiol., 64, 666 671.
35. Onimaru, H. Homma, I. (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci., 23, 1478 1486.
36. Onimaru, H. Homma, I. (2006) Point: Counterpoint: The parafacial respiratory group (pFRG)/pre-Botzinger complex (preBotC) is the primary site of respiratory rhythm generation in the mammal. Point: the PFRG is the primary site of respiratory rhythm generation in the mammal. J. Appl. Physiol., 100, 2094 2095.
37. Potts, J.T., Rybak, I.A. Paton, J.F. (2005) Respiratory rhythm entrainment by somatic afferent stimulation. J. Neurosci., 25, 1965 1978.
38. Prabhakar, N.R. Jacono, F.J. (2005) Cellular and molecular mechanisms associated with carotid body adaptations to chronic hypoxia. High Alt. Med. Biol., 6, 112 120.
39. Prabhakar, N.R. Peng, Y.J. (2004) Peripheral chemoreceptors in health and disease. J. Appl. Physiol., 96, 359 366.
40. Rekling, J.C. Feldman, J.L. (1998) PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol., 60, 385 405.
41. Rybak, I.A., Shevtsova, N.A., Paton, J.F., Dick, T.E., St-John, W.M., Morschel, M. Dutschmann, M. (2004) Modeling the ponto-medullary respiratory network. Resp. Physiol. Neurobiol., 143, 307 319.
42. Sangha, S., Varshney, N., Fras, M., Smyth, K., Rosenegger, D., Parvez, K., Sadamoto, H. Lukowiak, K. (2004) Memory, reconsolidation and extinction in Lymnaea require the soma of RPeD1. Adv. Exp. Med. Biol., 551, 311 318.
43. Smit, A.B., Syed, N.I., Schaap, D., van Minnen, J., Klumperman, J., Kits, K.S., Lodder, H., van der Schors, R.C., van Elk, R., Sorgedrager, B., Brejc, K., Sixma, T.K. Geraerts, W.P. (2001) A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature, 411, 261 268.
44. Smith, J.C., Ellenberger, H.H., Ballanyi, K., Richter, D.W. Feldman, J.L. (1991) Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science, 254, 726 729.
45. Sokolov, V.A. Kamardin, N.N. (1977) The relation of impulse frequency in the osphradial nerve to the concentration of oxygen and inulin in liquid passing over the osphradium of the pond snail. Vestnik. Leningr. Univ. Biol., 1, 87 90.
46. Stulbarg, M.S., Winn, W.R. Kellett, L.E. (1989) Bilateral carotid body resection for the relief of dyspnea in severe chronic obstructive pulmonary disease. Physiologic and clinical observations in three patients. Chest, 95, 1123 1128.
47. Syed, N.I. Winlow, W. (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea-Stagnalis (L). Comp. Biochem. Physiol. A, 93, 633 644.
48. Syed, N.I. Winlow, W. (1991) Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J. Exp. Biol., 158, 37 62.
49. Syed, N.I., Bulloch, A.G. Lukowiak, K. (1990) In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science, 250, 282 285.
50. Syed, N.I., Harrison, D. Winlow, W. (1991) Respiratory behavior in the pond snail Lymnaea-Stagnalis.1. Behavioral-analysis and the identification of motor neurons. J. Comp. Physiol. A Sens. Neural Behav. Physiol., 169, 541 555.
51. Syed, N.I., Hasan, Z. Lovell, P. (1999) In vitro reconstruction of neuronal circuits: a simple model system approach. In Windhorst, U. Johnsson, H. (Eds), Modern Techniques in Neuroscience Research, Springer, Berlin. pp. 361 377.
52. Szlyk, P.C. Jennings, D.B. (1987) Respiration in awake cats: sympathectomy and deafferentation of carotid bifurcations. J. Appl. Physiol., 62, 932 940.
53. Turner, D.L. Mitchell, G.S. (1997) Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J. Physiol., 499 (2 543 550.
54. Van Vliet, B.N. West, N.H. (1992) Functional characteristics of arterial chemoreceptors in an amphibian (Bufo marinus). Resp. Physiol., 88, 113 127.
55. Walcourt-Ambakederemo, A. Winlow, W. (1994) 5-HT receptors on identified Lymnaea neurones in culture: pharmacological characterization of 5-HT2 receptors. Gen. Pharmacol., 25, 1079 1092.
56. Wedemeyer, H. Schild, D. (1995) Chemosensitivity of the osphradium of the pond snail Lymnaea stagnalis. J. Exp. Biol., 198, 1743 1754.
57. Wilson, R.J., Vasilakos, K. Remmers, J.E. (2006) Phylogeny of vertebrate respiratory rhythm generators: The Oscillator Homology Hypothesis. Resp. Physiol. Neurobiol., 154, 47 60.
58. Woodin, M.A., Munno, D.W. Syed, N.I. (2002) Trophic factor-induced excitatory synaptogenesis involves postsynaptic modulation of nicotinic acetylcholine receptors. J. Neurosci., 22, 505 514.
59. Wu, M., Haxhiu, M.A. Johnson, S.M. (2005) Hypercapnic and hypoxic responses require intact neural transmission from the pre-Botzinger complex. Resp. Physiol. Neurobiol., 146, 33 46.
60. Zhang, M. Nurse, C.A. (2004) CO2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. J. Neurophysiol., 92, 3433 3445.
61. Zhang, M., Zhong, H., Vollmer, C. Nurse, C.A. (2000) Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. J. Physiol., 525 (1 143 158.