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Historical Overview: The Search for inhibitory neurons and their function

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Excitatory-Inhibitory Balance
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Abstract

Even though inhibition had long been recognized as a distinct process in the nervous system (see Sherrington1), the discovery of inhibitory synapses had to wait until the middle of the 20th century. In mammalian motoneurons, Eccles and his associates recorded inhibitory postsynaptic potentials (IPSPs) that form a mirror image of excitatory postsynaptic potentials (EPSPs)2.

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References

  1. Sherrington, C.S. (1906) Integrative Action of the Nervous System. (Yale Univ. Press, New Haven).

    Google Scholar 

  2. Brock, L.G., Coombs, J.S. and Eccles, J.C. (1952) The recording of potentials from motoneurones with an intracellular electrode. J. Physiol. (Lond.) 117, 431–460.

    CAS  Google Scholar 

  3. Eccles, J.C. (1962) Spinal neuron: synaptic connexions in relation to chemical transmitters and pharmacological responses. Proc. First Intern. Pharmacol. Meeting 8157–182.

    CAS  Google Scholar 

  4. Eccles, J.C., Fatt, P. and Koketsu, K. (1954) Cholinergic and inhibitory synapses in a pathway from motor axon collaterals to motoneurons. J. Physiol. (Lond.) 126,524–564.

    CAS  Google Scholar 

  5. Eccles, J.C., Fatt, P. and Landgren, S. (1956) Central pathway for direct inhibitory action on impulses in large afferent nerve fibres to muscle. J. Neurophysiol. 19, 75–98,

    PubMed  CAS  Google Scholar 

  6. Ito, M. and Yoshida, M. (1964) The cerebellar-evoked monosynaptic inhibition of Deiters neurones. Experientia. 40, 762–764.

    Google Scholar 

  7. Aprison, M.H. and Werman, R. (1965) The distribution of glycine in cat spinal cord and roots. Life Sci. 4, 2075–2083.

    Article  PubMed  CAS  Google Scholar 

  8. Obata, K. Ito, M., Ochi, R. and Sato, N. (1967) Pharmacological properties of the postsynaptic inhibition by Purkinje cell axons and the action of g-aminobutryic acid on Deiters neurons. Exp. Brain Res. 4, 43–57

    Article  PubMed  CAS  Google Scholar 

  9. Kuffler, S.W. and Edwards, C. (1958) Mechanism of gamma-aminobutyric acid (GABA) action and its relation to synaptic inhibition. J. Neurophysiol. 21, 589–610.

    PubMed  CAS  Google Scholar 

  10. Watanabe. M„ Maemura. K„ Kanbara, K., Tamayama, T. and Hayasaki, H. (2002) GABA and GABA receptors in the central nervous system and other organs. Int. Rev. Cytol. 213, 1–47.

    Article  PubMed  CAS  Google Scholar 

  11. Eccles, J.C., Eccles, R.M., Iggo, A. and Ito, M. (1961) Distribution of recurrent inhibition among motoneurones. J. Physiol. (Lond.) 159, 479–499.

    CAS  Google Scholar 

  12. Windhorst, U. (1990) Activation of Renshaw cells. Prog. Neurobiol. 35, 135–179.

    CAS  Google Scholar 

  13. Maltenfort, M.G., Heckman, C.J. and Rymer, W.Z. (1998) Decorrelating actions of renshaw intemeurons on the firing of spinal motoneurons within a motor nucleus: a simulation study. J. Neurophysiol. 80, 309–323.

    PubMed  CAS  Google Scholar 

  14. Andersen, P. and Eccles, J.C. (1962) Inhibitory phasing of neuronal discharge. Nature 196, 645–647.

    Article  PubMed  CAS  Google Scholar 

  15. Wilson, D.M. and Wardron, I. (1968) Models for the generation of the motor ouutput pattern in flying locusts. Proc. IEEE 56,1058–1064.

    Article  Google Scholar 

  16. Lundberg, A. (1981) Half-center revisited. In: Regulatory Pathway of the CNS Principles of Motion and Organization, eds. J. Szentagothai, M. Parkovits, and J. Hamori. Adv. Physiol. Sci. 1,155–167.

    Google Scholar 

  17. Parker, D. and Grillner, S. (2000) Neuronal mechanisms of synaptic and network plasticity in the lamprey spinal cord. Prog. Brain Res. 125, 381–398.

    Article  PubMed  CAS  Google Scholar 

  18. Butt, S.J.B., Lebret, J.M. and Liehn, O. (2002) Organization of left-right coordination in the mammaian locomotor network. Brain Res. Rev. 40, 107–117.

    Article  PubMed  Google Scholar 

  19. Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G. and Jefferys, J.G. (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol (Lond.) 493, 471–484.

    CAS  Google Scholar 

  20. Soto-Trevino, C., Thoroughman, K.A., Marder, E. and Abbott, L.F. (2001) Activity-dependent modification of inhibitory synapses in models of rhythmic neural networks. Nat. Neurosci. 4, 297–303.

    Article  PubMed  CAS  Google Scholar 

  21. Selverston AI, Moulins M. (1985) Oscillatory neural networks. Annu Rev Physiol. 47, 29–48.

    Article  PubMed  CAS  Google Scholar 

  22. Arshavsky, Y.I., (2003) Cellular and network properties in the functioning of the nervous system : from central patter generators to cognition. Brain.Res. Rec 41, 229–267.

    Article  Google Scholar 

  23. Koulakov, A.A., Raghavachari, S., Kepecs, A. and Lisman, J.E. (2002) Model for a robust neural integrator. Nat. Neurosci. 5, 775–782.

    Article  PubMed  CAS  Google Scholar 

  24. Cannon, S.C., Robinson, D.A. and Shamma, S. (1983) A proposed neural network for the integrator of the oculomotor system. Biol. Cybern. 49, 127–136.

    Article  PubMed  CAS  Google Scholar 

  25. Cannon, S.C. and Robinson, D.A. (1985.25) An improved neural-network model for the neural integrator of the oculomotor system: more realistic neuron behavior. Biol. Cybern. 53, 93–108.

    Article  PubMed  CAS  Google Scholar 

  26. Holstein, G.R., Martinelli, G.P. and Cohen, B. (1999) The ultrastructure of GABA-immunoreactive vestibular commissural neurons related to velocity storage in the monkey. Neuroscience 93, 171–181.

    Article  PubMed  CAS  Google Scholar 

  27. Fujita M. (1982) Adaptive filter model of the cerebellum. Biol. Cybern. 45, 195–206.

    Article  PubMed  CAS  Google Scholar 

  28. Marr, D.A. (1969) A theory of cerebellar cortex. J. Physiol (Lond.) 202, 437–470.

    CAS  Google Scholar 

  29. Albus, J.S. (1971) A theory of cerebellar function. Math. Biosci. 10, 25–26.

    Article  Google Scholar 

  30. Braitenberg, V. and Onesto, N. (1962) The cerebellar cortex as a timing organ. Discussion of a hypothesis. Proc. 1st Intern. Conf. Med. Cybern. (Giannini: Naples, Italy),pp 1-19.

    Google Scholar 

  31. Clifford, C.W.G. and Ibbotson, M.R. (2003) Fundamental mechanisms of visual motion detection: models, cells and functions. Progr. Neurobiol. 68, 409–437.

    Article  Google Scholar 

  32. Torre, V. and Poggio, T. (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc. R. Soc. Lond. B 202, 409–416.

    Article  Google Scholar 

  33. Koch, C, Poggio, T. and Torre, V. (1983) Non-linear interactions in a dendritic tree: localization, timing and role in information processing. Proc. Natl. Acad. Sci. USA 80, 2799–2802.

    Article  PubMed  CAS  Google Scholar 

  34. Eccles, M., Ito, M. and Szentagothai J. (1967) The Cerebellum as a Neuronal Machine. (Springer-Verlag: New York), p 209.

    Google Scholar 

  35. Ito, M. (2002) Controller-regulator model of the central nervous system. J. Integrative Neurosci. 1, 129–143.

    Article  Google Scholar 

  36. Yoshida, M. and Precht, W. (1971) Monosynaptic inhibition of neurons in the substantia nigra by caudate-nigral fibers. Brain Res. 32, 225–228.

    Article  PubMed  CAS  Google Scholar 

  37. Ueki, A., Uno, M., Anderson, M. and Yoshida, M. (1977) Monosynaptic inhibition of thalamic neurons produced by stimulation of the substantia nigra Experientia 33, 1480–1481.

    Article  PubMed  CAS  Google Scholar 

  38. Kaji R. (2001) Basal ganglia as a sensory gating devise for motor control, J. Med. Invest. 48, 142–146.

    PubMed  CAS  Google Scholar 

  39. Hikosaka O., Takikawa Y., Kawagoe R. (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80, 953–978.

    PubMed  CAS  Google Scholar 

  40. Hikosaka, O., Takikawa, Y., and Kawagoe, R. (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80, 953–978.

    PubMed  CAS  Google Scholar 

  41. Scheibel, M.F. and Scheibel, A.B. (1958) Structural substrates for integrating patterns in the brain stem reticular core. In: Reticular Formation of the Brain, eds. H.H. Jasper et al. Little, Brown & Co. Boston

    Google Scholar 

  42. Ito, M., Udo, M. and Mano, N. (1970) Long inhibitory and excitatory pathways converging onto cat reticular and Deiters’ neurons and their relevance to reticulofugal axons. J. Neurophysiol. 33, 210–226.

    PubMed  CAS  Google Scholar 

  43. Takakusaki, K., Kohyama, J., Matsuyama, K. and Mori, S. (2001) Medullary reticulospinal tract mediating the generalized motor inhibition in cats: parallel inhibitory mechanisms acting on motoneurons and on interneuronal transmission in reflex pathways. Neuroscience 103, 511–527.

    Article  PubMed  CAS  Google Scholar 

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Ito, M. (2004). Historical Overview: The Search for inhibitory neurons and their function. In: Hensch, T.K., Fagiolini, M. (eds) Excitatory-Inhibitory Balance. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0039-1_1

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  • DOI: https://doi.org/10.1007/978-1-4615-0039-1_1

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4895-5

  • Online ISBN: 978-1-4615-0039-1

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