Advertisement

Synaptic Plasticity and Respiratory Control

  • Chi-Sang Poon

Abstract

In the past two decades there have been considerable advances in the understanding of the neural mechanisms of learning and memory in the mammalian higher brain. A preeminent view based upon the classical model of Hebb[27] holds that learning and memory may result from activity-dependent modifications of neural transmission at certain chemical synaptic junctions. Generally referred to as synaptic plasticity, such neuronal modifications are widely believed to occur in infancy and, to some extent, throughout adulthood. One of the best known examples of such synaptic modification is hippocampal long-term potentiation (LTP) of neural transmission which can be robustly induced by a brief period of tetanic (high-frequency) afferent stimulation, both in vivo and in vitro[3],[8],[9]. Recently, many other forms of synaptic plasticity have been identified in the hippocampus and other brain structures[4],[33],[37],[38]. it thus appears that synaptic plasticity is probably a generic property of many types of neurons which may be expressed throughout the mammalian central nervous system and may subserve a wide variety of neural functions.

Keywords

Synaptic Plasticity Ventilatory Response Respiratory Control Nucleus Tractus Solitarius Synaptic Strength 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Åstrom, K.J. and Wittenmark,. On self-tuning regulators. Automatica 9:185–199, 1973.CrossRefGoogle Scholar
  2. 2.
    Barnes, C.A., Bindman, L.J., Dudai, Y., Frégnac, Y., Ito, M., Knöpfel, T., Lisberger, S.G., Morris, R.G.M., Moulins, M., Movshon, J.A., Singer, W., and Squire, L.R. Group Report: Relating activity-dependent modifications of neuronal function to changes in neural systems and behavior. In A.I. Selverston and P. Ascher (Eds.), Cellular and Molecular Mechanisms underlying Higher Neural Functions, New York: Wiley, 1994, pp. 81–110.Google Scholar
  3. 3.
    Baudry, M. and J.L. Davis. Long-term Potentiation: A Debate of Current Issues. Cambridge, MA: MIT Press, 1990.Google Scholar
  4. 4.
    Baudry, M., Thompson, R.F. and Davis, J.L. Synaptic Plasticity: Molecular, Cellular, and Functional Aspects. Cambridge, MA: MIT Press, 1993.Google Scholar
  5. 5.
    Benchetrit, G. and F. Bertrand. A short-term memory in the respiratory centers: statistical analysis. Respir. Physiol. 23:147–158, 1975.PubMedCrossRefGoogle Scholar
  6. 6.
    Berkenbosch, A., J.G. Bovill, A. Dahan. J. DeGoede, and I.C.W. Olievier. The ventilatory CO2 sensitivities from Read’s rebreathing method and the stead-state method are not equal in man. J. Physiol. (London) 411:367–377, 1989.Google Scholar
  7. 7.
    Bisgard. G.E. and J.A. Neubauer. Peripheral and central effects of hypoxia. In: J.A. Dempsey and A.I. Pack (Eds.), Regulation of Breathing, 2nd ed., Lung Biology in Health and Disease, Vol. 79, 1995. pp. 617–668.Google Scholar
  8. 8.
    Bliss, T.V.P. and G.L. Collingridge. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39, 1993.PubMedCrossRefGoogle Scholar
  9. 9.
    Bliss, T.V.P. and T. Lømo. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (London) 232:331–356, 1973.Google Scholar
  10. 10.
    Bourke, D.L. and A. Warley. The steady-state and rebreathing methods compared during morphine administration in humans. J. Physiol. (London) 419:509–517, 1989.Google Scholar
  11. 11.
    Brown, T.H., E.W. Kairiss, and C.L. Keenan. Hebbian synapses: biophysical mechanisms and algorithms. Ann. Rev. Neurosci. 13:475–511, 1990.PubMedCrossRefGoogle Scholar
  12. 12.
    Byrne, J.H. Cellular analysis of associative learning. Physiol. Rev. 67:329–439, 1987.PubMedGoogle Scholar
  13. 13.
    Casaburi, R., B.J. Whipp, K. Wasserman, and R.W. Stremel. Ventilatory control characteristics of the exercise hyperpnea as discerned from dynamic forcing techniques. Chest 73:, Suppl.:280S–283S, 1978.Google Scholar
  14. 14.
    Debanne, D. and S.M. Thompson. Calcium: a trigger for long-term depression and potentiationin the hippocampus. News in Physiol. Sci. 9:256–260, 1994.Google Scholar
  15. 15.
    Duffin, J., K. Ezure, and J. Lipski. Breathing rhythm generation: focus on the rostral ventrolateral medulla. News in Physiol. Sci. 10:133–140, 1995.Google Scholar
  16. 16.
    Eldridge, F.L. The North Carolina respiratory model: A multipurpose model for studying the control of breathing. (This volume).Google Scholar
  17. 17.
    Eldridge, F.L. and Millhorn, D.E. Oscillation, gating, and memory in the respiratory control system. In N.S. Cherniack and J.G. Widdicombe (Eds.), Handbook of Physiology, The Respiratory System. Control of Breathing. Bethesda, MD: American Physiological Society, 1986, sect. 3, Vol. II, part I, p. 93–114.Google Scholar
  18. 18.
    Fortin, G., J.C. Velluti, M. Denavit-Saubié, and J. Champagnat. Responses to repetititive afferent activity of rat solitary complex neurons isolated in brainstem slices. Neurosci. Lett. 147:89–92, 1992.PubMedCrossRefGoogle Scholar
  19. 19.
    Fregosi, R.F. Short-term potentiation of breathing in humans. J. Appl. Physiol. 71, 892–899, 1991.PubMedGoogle Scholar
  20. 20.
    Fregosi, R.FF. and G.S. Mitchell. Long-term facilitation of inspiratory intercostal nerve activity following carotid sinus nerve stimulation in cats. J. Physiol. (London) 477:469–479, 1994.Google Scholar
  21. 21.
    Gallego, J., J. Ankaoua, M. Lethielleux, B. Chambille, G. Vardon, and C. Jacquemin. Retention of ventilatory pattern learning in normal subjects. J. Appl. Physiol. 61:1–6, 1986.PubMedGoogle Scholar
  22. 22.
    Gallego, J. and P. Perruchet. Classical conditioning of ventilatory responses in humans. J. Appl. Physiol. 70:676–682, 1991.PubMedGoogle Scholar
  23. 23.
    Georgopoulos, D., S. Walker, and N.R. Anthonisen. Effect of sustained hypoxia on ventilatory response to CO2 in normal adults. J. Appl. Physiol. 68:891–896, 1990.PubMedGoogle Scholar
  24. 24.
    Gesell, R., Brassfield, C.R., and Hamilton, M.A. An acid-neurohumoral mechanism of nerve cell activation. Am. J. Physiol. 136:604–608, 1942.Google Scholar
  25. 25.
    Gesell, R. and Hamilton, M.A. Reflexogenic components of breathing. Am. J. Physiol. 133:694–719, 1941.Google Scholar
  26. 26.
    Hawkins, R.D., E.R. Kandel and S.A. Siegelbaum. Learning to modulate transmitter release: Themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16:625–665, 1993.PubMedCrossRefGoogle Scholar
  27. 27.
    Hebb, D.O. The Organization of Behavior. New York: Wiley, 1949.Google Scholar
  28. 28.
    Ito, M. The Cerebellum and Neural Control. NY: Raven Press, 1984.Google Scholar
  29. 29.
    Ito, M., M. Sakurai, and P. Tongroach. Climbing fiber induced depression of both mossy fiber responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. (London) 324:113–134, 1982.Google Scholar
  30. 30.
    Kamlya, H. and R.S. Zucker. Residual Ca2+ and short-term synaptic plasticity. Nature 371:603–606, 1994.CrossRefGoogle Scholar
  31. 31.
    Khoo, M.C.K., R.E. Kronauer, K.P. Strohl, and A.S. Slutsky. Factors induing periodic breathing: a general model. J. Appl. Physiol. 53:644–659, 1982.PubMedGoogle Scholar
  32. 32.
    Kirkwood, A. and M.F. Bear. Hebbian synapses in visual cortex. J. Neurosci. 14:1634–1645, 1994.PubMedGoogle Scholar
  33. 33.
    Kirkwood, A., Dudek, S.M., Gold, J.T., Aizenman, C.D., and Bear, M.F. Common forms of synaptic plasticity in hippocampus and neocortex in vitro. Science 260, 1518–1521, 1993.PubMedCrossRefGoogle Scholar
  34. 34.
    Kuo, B.C. Automatic Control Systems. 2nd ed., Englewood Cliffs, NJ: Prentice-Hall, 1972.Google Scholar
  35. 35.
    Li, Y., Erzurumlu, R.S., Chen, C., Jhaveri, S., and Tonegawa, S. Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. (1994). Cell 76, 427–437, 1994.PubMedCrossRefGoogle Scholar
  36. 36.
    Magleby, K.L. Synaptic transmission, facilitation, augmentation, potentiation, depression. In: G. Edelman (Ed.), Encyclopedia of Neuroscience, Vol. 2., pp. 1170–1174, Boston: Biekhauser, 1987.Google Scholar
  37. 37.
    Malenka, R.C. Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78:535–538, 1994.PubMedCrossRefGoogle Scholar
  38. 38.
    Malenka, R.C. and R.A. Nicoll. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends in Neural Sci. 16:521–527, 1993.CrossRefGoogle Scholar
  39. 39.
    Martin, P.A. and G.S. Mitchell. Long-term modulation of the exercise ventilatory response in goats. J. Physiol. (London) 470:601–617, 1993.Google Scholar
  40. 40.
    Mazza, E., N.H. Edelman and J.A. Neubauer. Intrinsic effects on membrane potential and input resistance of chemical hypoxia on cultured neurons from the rostral ventral lateral medulla (RVLM). Soc. Neurosci. Abstr. 21:1881, 1995.Google Scholar
  41. 41.
    Millhorn, D.E. Stimulation of raphe (obscurus) nucleus causes long-term potentiation of phrenic nerve activity in cat. J. Physiol. (London) 381:169–179, 1986.Google Scholar
  42. 42.
    Narendra, K.S. and Annaswamy, A.M. (1989). Stable Adaptive Systems. Englewood Cliffs: Prentice Hall.Google Scholar
  43. 43.
    Pavlov, I.P. Lectures on Conditioned Reflexes — Twenty-Five Years of Objective Study of the Higher Nervous Activity (Behavior) of Animals, translated by W.H. Gantt. New York: International Publishers. 1928.Google Scholar
  44. 44.
    Poon, C.-S. Optimal control of ventilation in hypoxia, hypercapnia and exercise. In B.J. Whipp and D.M. Wiberg (Eds.), Modelling and Control of Breathing. New York: Elsevier. 1983, pp. 189–196.Google Scholar
  45. 45.
    Poon. C.-S. Ventilatory control in hypercapnia and exercise: optimization hypothesis. J. Appl. Physiol. 62, 2447–2459. 1987.PubMedGoogle Scholar
  46. 46.
    Poon, C.-S. Optimization character of brainstem respiratory neurons: a cerebral neural network model. Biol. Cybern. 66, 9–17, 1991.PubMedCrossRefGoogle Scholar
  47. 47.
    Poon, C.-S. Introduction: Optimization hypothesis in the control of breathing. In Y. Honda. Y. Miyamoto. K. Konno, and J.G. Widdicombe (Eds.). Control of Breathing and its Modeling Perspective. New York: Plenum, 1992, pp. 371–384.Google Scholar
  48. 48.
    Poon, C.-S. Potentiation of exercise ventilatory response by CO2 and dead space loading. J. Appl. Physiol. 73,591–595. 1992.PubMedGoogle Scholar
  49. 49.
    Poon, C.-S. Adaptive neural network that subserves optimal homeostatic control of breathing. Annals of Biomed. Engr. 21, 501–508, 1993.CrossRefGoogle Scholar
  50. 50.
    Poon, C.-S. Hebbian synaptic plasticity: a neural mechanism of supervised learning and adaptive control. In B.W. Patterson (Ed.), Modeling and Control in Biomedical Systems, Madison, WI: Omnipress, 1994. pp. 497–500.Google Scholar
  51. 51.
    Poon, C.-S. Respiratory models and control. In J.D. Bronzino (Ed.), Biomedical Engineering Handbook, Boca Raton, FL: CRC Press, 1995, pp. 2404–2421.Google Scholar
  52. 52.
    Poon, C.-S. Learning to optimize performance: Lessons from a neural control system. Preprints of the 6th IFAC/IFIP/IFORS/IEA Symposium on Analysis, Design and Evaluation of Man-Machine Systems, Cambridge, MA, 1995, pp. 499–504.Google Scholar
  53. 53.
    Poon. C.-S. Self-tuning optimal regulation of respiratory motor output by Hebbian covariance learning. Neural Networks, 1996 (acceped for publication in a special issue on “Four major hypotheses in neuroscience”).Google Scholar
  54. 54.
    Poon, C.-S. and J.G. Grenne. Control of exercise hyperpnea during hypercapnia in humans. J. Appl. Physiol. 59:792–797, 1985.PubMedGoogle Scholar
  55. 55.
    Poon, C.-S., Lin, S.L., and Knudson, O.B. Optimization character of inspiraotry neural drive. J. Appl. Physiol. 72:2005–2017, 1992.PubMedGoogle Scholar
  56. 56.
    Poon. C.-S., Li, Y., Li, S.X. and Tonegawa, S. Respiratory rhythm is altered in neonatal mice with malfunctional NMDA receptors. FASEB J. 8, A389, 1994.Google Scholar
  57. 57.
    Priban, I.P. An analysis of some short-term patterns of breathing in man at rest. J. Physiol. (London) 166:425–434, 1963.Google Scholar
  58. 58.
    Read, D.J.C. A clinical method for assessing the ventilatory response to carbon dioxide. Australasian Annals Med., 16:20–32, 1967.Google Scholar
  59. 59.
    Richter, D.W., A. Bischoff, K. Anders, M. Bellingham, and U. Windhorst. Response of the medullary respiratory network of the rat to hypoxia. J. Physiol. (London) 470:23–33, 1993.Google Scholar
  60. 60.
    Robbins, P.A. Hypoxic ventilatory decline: site of action. J. Appl. Physiol. 79:373–374, 1995.PubMedGoogle Scholar
  61. 61.
    Schmidt-Nielsen, K. How are control systems controlled? Am. Scientist. 82, 38–44, 1994.Google Scholar
  62. 62.
    Sidney, D.A. and Poon, C.-S. Ventilatory responses to dead space and CO2 breathing under inspiratory resistive load. J. Appl. Physiol. 78, 555–561, 1995.PubMedGoogle Scholar
  63. 63.
    Somjen, G.G. The missing error signal — regulation beyond negative feedback. News in Physiol. Sci. 7, 184–185, 1992.Google Scholar
  64. 64.
    Swanson, G.D. and J.W. Bellville. Step changes in end-tidal CO2: methods and implications. J. Appl. Physiol. 39:377–385, 1975.PubMedGoogle Scholar
  65. 65.
    Thomas, A.J., L. Friedman, C.N. MacKenzie, and K.P. Strohl. Modification of conditioned apneas in rats: evidence for cortical involvement. J. Appl. Physiol. 78:1215–1218, 1995.PubMedGoogle Scholar
  66. 66.
    Wagner, P.G. and Eldridge, F.L. Development of short-term potentiation of respiration. Respirat. Physiol. 83:129–140, 1991.CrossRefGoogle Scholar
  67. 67.
    Wasserman, K., Whipp, B.J. and Casaburi, R. Respiratory control during exercise. In N.S. Cherniack and J.G. Widdicombe (Eds.), Handbook of Physiology, The Respiratory System. Control of Breathing. Bethesda, MD: American Physiological Society. 1986, sect. 3, Vol. II, part II p. 595–620.Google Scholar
  68. 68.
    Yamamoto, W.S. Mathematical analysis of the time course of alveolar CO2. J. Appl. Physiol. 15, 215–219, 1960.PubMedGoogle Scholar
  69. 69.
    Younes, M. The physiological basis of central apnea and periodic breathing. Curr. Pulmonol. 10:265–326, 1989.Google Scholar
  70. 70.
    Zhou, Z., Champagnat, J. and Poon, C.-S. Synaptic short-term depression in nucleus tractus solitarius (NTS) of rat brain stem in vitro. FASEB J. 9, A3283, 1995.Google Scholar
  71. 71.
    Zhou, Z., Champagnat, J. and Poon, C.-S. Intracellular calcium is required for the maintenance but not induction of long-term depression in nucleus tractus solitarius. Soc. Neurosci. Abstr. 21:263, 1995.Google Scholar

Copyright information

© Plenum Press 1996

Authors and Affiliations

  • Chi-Sang Poon
    • 1
  1. 1.Harvard-MIT Division of Health Sciences and TechnologyMassachusetts Institute of TechnologyCambridge

Personalised recommendations