Role of synaptic inhibition in turtle respiratory rhythm generation

Journal of Physiology

Volumn 544, Issue 1, 2002, Pages 253-265

  Johnson, Stephen M ^a   Wilkerson, Julia E R ^a,b   Wenninger, Michael R ^a   Henderson, Daniel R ^a   Mitchell, Gordon S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; BICUCULLINE; CARBON DIOXIDE; GLYCINE RECEPTOR ANTAGONIST; MU OPIATE RECEPTOR; STRYCHNINE; GLYCINE RECEPTOR;

ADOLESCENT; ANIMAL TISSUE; BRAIN STEM; BREATHING PATTERN; CARBON DIOXIDE TENSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EXHALATION; HYPOGLOSSAL NERVE; IN VITRO STUDY; INHALATION; MOTONEURON; NERVE CONDUCTION; NONHUMAN; PACEMAKER; PRIORITY JOURNAL; REVIEW; SPINAL CORD; SYNAPTIC INHIBITION; TURTLE; ACTION POTENTIAL AMPLITUDE; ADULT; ARTICLE; GABAERGIC SYSTEM; RESPIRATORY FUNCTION; RESPIRATORY NERVE CELL;

ANIMALS; BICUCULLINE; BRAIN STEM; CARBON DIOXIDE; GABA ANTAGONISTS; GLYCINE AGENTS; HYDROGEN-ION CONCENTRATION; NEURAL INHIBITION; PERIODICITY; RECEPTORS, GABA-A; RECEPTORS, GABA-B; RECEPTORS, GLYCINE; RECEPTORS, OPIOID, MU; RESPIRATORY MECHANICS; SPINAL CORD; STRYCHNINE; SYNAPSES; TURTLES;

EID: 0036794549     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.019687     Document Type: Review

References (63)

1. AKOPIAN, A., GABRIEL, R. & WITKOVSKY, P. (1998). Calcium released from intracellular stores inhibits GABAA-mediated currents in ganglion cells of the turtle retina. Journal of Neurophysiology 80, 1105-1115.
2. BOU-FLORES, C. & BERGER, A.J. (2001). Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. Journal of Neurophysiology 85, 1543-1551.
3. BROCKHAUS, J. & BALLANYI, K. (1998). Synaptic inhibition in the isolated respiratory network of neonatal rats. European Journal of Neuroscience 10, 3823-3839.
4. BÜSSELBERG, D., BISCHOFF, A. M., PATON, J. F. R. & RICHTER, D. W. (2001). Reorganisation of respiratory network activity after loss of glycinergic inhibition. Pfügers Archiv 441, 444-449.
5. BUTERA, R. J., RINZEL, J. & SMITH, J. C. (1999a). Models of respiratory rhythm generation in the pre-Bötzinger complex. I. Bursting pacemaker neurons. Journal of Neurophysiology 81, 382-397.
6. BUTERA, R. J., RINZEL, J. & SMITH, J. C. (1999b). Models of respiratory rhythm generation in the pre-Bötzinger complex. II. Populations of coupled pacemaker neurons. Journal of Neurophysiology 81, 398-415.
7. CURRIE, S. N. & LEE, S. (1997). Glycinergic inhibition contributes to the generation of rostral scratch motor patterns in the turtle spinal cord. Journal of Neuroscience 17, 3323-3333.
8. DEL NEGRO, C. A., MORGADO-VALLE, C. & FELDMAN, J. L. (2002). Respiratory rhythm: an emergent network property? Neuron 34, 821-830.
9. DOUSE, M. A. & MITCHELL, G. S. (1990). Episodic respiratory related discharge in turtle cranial motoneurons: in vivo and in vitro studies. Brain Research 536, 297-300.
10. DUFFIN, J., EZURE, K. & LIPSKI, J. (1995). Breathing rhythm generation: focus on the rostral ventrolateral medulla. News in Physiological Science 10, 133-140.
11. FELDMAN, J. L. & CLELAND, C. L. (1982). Possible roles of pacemaker neurons in mammalian respiratory rhythmogenesis. In Cellular Pacemakers, ed. CARPENTER, D.O., pp. 101-119. John Wiley and Sons, NY, USA.
12. FELDMAN, J. L. & SMITH, J. C. (1989).Cellular mechanisms underlying modulation of breathing patterns in mammals. Annals of the New York Academy of Science 563, 114-130.
13. FELDMAN, J. L., SMITH, J. C., ELLENBERGER, H. H., CONNELLY, C. A., LIU, G., GREER, J. J., LINDSAY, A. D. & OTTO, M. R. (1990). Neurogenesis of respiratory rhythm and pattern: emerging concepts. American Journal of Physiology 28, R879-886.
14. FELDMAN, J. L., SMITH, J. C., ELLENBERGER, H. H., FOURNIER, M. & CONNELLY, C. A. (1989). Breathing in mammals: rhythm and pattern. In Neuronal and Cellular Oscillators, ed. JACKLET, J. W., pp. 435-456. Marcel Dekker, NY, USA.
15. FUNK, G. D. & FELDMAN, J. L. (1995). Generation of respiratory rhythm and pattern in mammals: insights from developmental studies. Current Opinion in Neurobiology 5, 778-785.
16. GALANTE, R. J., KUBIN, L., FISHMAN, A. P. & PACK, A. I. (1996). Role of chloride-mediated inhibition in respiratory rhythmogenesis in an in vitro brainstem of a tadpole, Rana catesbeiana. Journal of Physiology 492, 545-558.
17. GANS, C. & HUGHES, G. M. (1967). The mechanism of lung ventilation in the tortoise Testudo graeca linné. Journal of Experimental Biology 47, 1-20.
18. GAUNT, A.S. & GANS, C. (1967) Mechanics of respiration in the snapping turtle, Chelydra serpentina (Linné). Journal of Morphology 128, 195-226.
19. GDOVIN, M. J., TORGERSON, C. S. & REMMERS, J. E. (1999). The fictively breathing tadpole brainstem preparation as a model for the development of respiratory pattern generation and central chemoreception. Comparative Biochemistry and Physiology A 124, 275-286.
20. GETTING, P.A. (1988). Comparative analysis of invertebrate central pattern generators. In Neural Control of Rhythmic Movements in Vertebrates, ed. COHEN, A. H., ROSSIGNOL, S. & GRILLNER, S., pp. 101-127. John Wiley and Sons, NY, USA.
21. GRAY, P. A., JANCZEWSKI, W. A., MELLEN, N., MCCRIMMON, D. R. & FELDMAN, J. L. (2001). Normal breathing requires pre-Bötzinger Complex neurokinin-1 receptor-expressing neurons. Nature Neuroscience 4, 927-930.
22. HAYASHI, F. & LIPSKI, J. (1992). The role of inhibitory amino acids in control of respiratory motor output in an arterially perfused rat. Respiration Physiology 89, 47-63.
23. 2 effects on respiratory discharge from a turtle brain stem preparation. Journal of Applied Physiology 84, 649-660.
24. JOHNSON, S. M., KOSHIYA, N. & SMITH, J. C. (2001a). Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Bötzinger complex 'island'. Journal of Neurophysiology 85, 1772-1776.
25. CO2-insensitive in turtle brainstem-spinal cord preparation. Respiration Physiology 113, 201-212.
26. JOHNSON, S. M., SMITH, J. C., FUNK, G. D. & FELDMAN, J. L. (1994). Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat. Journal of Neurophysiology 72, 2598-2608.
27. JOHNSON, S. M., WILKERSON, J. E. R., HENDERSON, D. R. & WENNINGER, M. R. (2001b). Role of synaptic inhibition in respiratory rhythm generation in turtle brainstems in vitro. Society for Neuroscience Abstracts 243, 4.
28. JONAS, P., BISCHOFBERGER, J. & SANDKÜHLER, J. (1998). Corelease of two fast neurotransmitters at a central synapse. Science 281, 419-424.
29. KIMURA, N., PERRY, S. F. & REMMERS, J. E. (1997). Strychnine eliminates reciprocation and augmentation of respiratory bursts of the in vitro frog brainstem. Neuroscience Letters 225, 9-12.
30. KOSHIYA, N. & SMITH, J. C. (1999). Neuronal pacemaker for breathing visualized in vitro. Nature 400, 360-363.
31. LARSON-PRIOR, L. J. & SLATER, N. T. (1988). GABA ergic inhibition and epileptiform discharges in the turtle hippocampus in vitro. Brain Research 460, 369-375.
32. 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. Nature Neuroscience 3, 600-607.
33. MCCRIMMON, D. R., RAMIREZ, J. M., ALFORD, S. & ZUPERKU, E. J. (2000). Unraveling the mechanism for respiratory rhythm generation. BioEssays 22, 6-9.
34. MCCUTCHEON, F. H. (1943). The respiratory mechanism in turtles. Physiological Zoology 3, 255-269.
35. A-mediated inhibition in controlling the responses of regular spiking cells in turtle visual cortex. Visual Neuroscience 18, 9-24.
36. MILSOM,W. K. & JONES, D. R. (1980). The role of vagal afferent information and hypercapnia in control of the breathing pattern in chelonia. Journal of Experimental Biology 87, 53-63.
37. PATON, J. F. R., RAMIREZ, J. M. & RICHTER, D. W. (1994). Mechanisms of respiratory rhythm generation change profoundly during early life in mice and rats. Neuroscience Letters 170, 167-270.
38. PATON, J. F.R. & RICHTER, D. W. (1995). Role of fast inhibitory synaptic mechanisms in respiratory rhythm generation in the maturing mouse. Journal of Physiology 484, 505-521.
39. PIERREFICHE, O., SCHWARZACHER, S. W., BISCHOFF, A. M. & RICHTER, D. W. (1998). Blockade of synaptic inhibition within the preBötzinger complex in the cat suppresses respiratory rhythm generation in vivo. Journal of Physiology 509, 245-254.
40. RAMIREZ, J. M., QUELLMALZ, U. J. A. & RICHTER, D. W. (1996). Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice. Journal of Physiology 491, 799-812.
41. RAMIREZ, J. M. & RICHTER, D. W. (1996). The neuronal mechanisms of respiratory rhythm generation. Current Opinion in Neurobiology 6, 817-825.
42. RAMIREZ, J. M., SCHWARZACHER, S. W., PIERREFICHE, O., OLIVERA, B. M. & RICTHER, D. W. (1998). Selective lesioning of the cat pre-Bötzinger complex in vivo eliminates breathing but not gasping. Journal of Physiology 507, 895-907.
43. RAMIREZ, J. M., TELGKAMP, P., ELSEN, F. P., QUELLMALZ, U. J. A. & RICHTER, D. W. (1997). Respiratory rhythm generation in mammals: synaptic and membrane properties. Respiration Physiology 110, 71-85.
44. REKLING, J. C., CHAMPAGNAT, J. & DENAVIT-SAUBIE, M. (1996). Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro. Journal of Neurophysiology 75, 795-8 10.
45. REKLING, J. C. & FELDMAN, J. L. (1998). Pre-Bötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annual Review of Physiology 60, 385-405.
46. RICHTER, D. W., BALLANYI, K. & RAMIREZ, J. M. (1997). Respiratory rhythm generation. In Neural Control of the Respiratory Muscles, ed. MILLER, A. D., BIANCHI, A. L. & BISHOP, B. P., pp. 119-130. CRC Press, USA.
47. RICHTER, D. W., BALLANYI, K. & SCHWARZACHER, S. (1992). Mechanisms of respiratory rhythm generation. Current Opinion in Neurobiology 2, 788-793.
48. RICHTER, D. W. & SPYER, K. M. (200 1). Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends in Neurosciences 8, 464-472.
49. Russo, R. E., NAGY, F. & HOUNSGAARD, J. (1998). Inhibitory control of plateau properties in dorsal horn neurones in the turtle spinal cord in vitro. Journal of Physiology 506, 795-808.
50. RYBAK, I. A., PATON, J. F.R. & SCHWABER, J. S. (1997). Modeling neural mechanisms for genesis of respiratory rhythm and pattern. II. Network models of the central respiratory pattern generator. Journal of Neurophysiology 77, 2007-2026.
51. RYBAK, I. A., ST JOHN, W. M. & PATON, J. F. R. (2001). Models of neuronal bursting behavior: implications for in vivo versus in vitro respiratory rhythmogenesis. In Frontiers in Modeling and Control of Breathing: Integration at Molecular, Cellular and Systems Levels, ed. POON, C. S., pp. 159-164. Klewer Press, NY, USA.
52. SCHMID, K., BÖHMER, G. & GEBAUER, K. (1991). Glycine receptor-mediated fast synaptic inhibition in the brainstem respiratory system. Respiration Physiology 84, 351-361.
53. SHAO, X. M. & FELDMAN, J. L. (1997). Respiratory rhythm generation and synaptic inhibition of expiratory neurons in the pre-Bötzinger complex: differential roles of glycinergic and GABAergic neural transmission. Journal of Neurophysiology 77, 1853-1860.
54. SILVER, R. B. & JACKSON, D. C. (1985). Ventilatory and acid-base responses to long-term hypercapnia in the freshwater turtle, Chrysemyspicta bellii. Journal of Experimental Biology 114, 661-672.
55. SMITH, J. C., BUTERA, R. J., KOSHIYA, N., DEL NEGRO, C., WILSON, C. G. & JOHNSON, S. M. (2000). Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model. Respiration Physiology 122, 131-147.
56. SMITH, J. C., ELLENBERGER, H. H., BALLANYI, K., RICHTER, D. W. & FELDMAN, J. L. (1991). Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254, 726-729.
57. SMITH, J. C. & FELDMAN, J. L. (1987). Central respiratory pattern generation studied in an in vitro mammalian brainstem-spinal cord preparation. In Respiratory Muscles and Their Neuromotor Control, ed. SEICK, G., GANDEVIA, S. C. & CAMERON, W. E., pp. 27-36. AR Liss, NY, USA.
58. SMITH, J. C., FUNK, G. D., JOHNSON, S. M. & FELDMAN, J. L. (1995). Cellular and synaptic mechanisms generating respiratory rhythm: insights from in vitro and computational studies. In Ventral Brainstem Mechanisms and Control of Respiration and Blood Pressure, ed. TROUTH, C. O., MILLIS, R., KIWULL-SCHONE, H. & SCHLAEFKE, M., pp. 463-496. Marcel Dekker, NY, USA.
59. TAKEDA, R., REMMERS, J. E., BAKER, J. P., MADDEN, K. P. & FARBER, J. P. (1986). Postsynaptic potentials of bulbar respiratory neurons of the turtle. Respiration Physiology 64, 149-160.
60. THOBY-BRISSON, M. & RAMIREZ, J. M. (2000). Role of inspiratory pacemaker neurons in mediating the hypoxic response of the respiratory network in vitro. Journal of Neuroscience 20, 5858-5866.
61. THOBY-BRISSON, M. & RAMIREZ, J. M. (2001). Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice. Journal of Neurophysiology 86, 104-112.
62. TORGERSON, C. S., GDOVIN, M. J. & REMMERS, J. E. (2001). Sites of respiratory rhythmogenesis during development in the tadpole. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 280, R913-920.
63. WILSON, R. J. A., VASILAKOS, K., HARRIS, M. B., STRAUS, C. & REMMERS, J. E. (2002). Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators. Journal of Physiology, 540,