Trends in Neurosciences
Volume 25, Issue 11, 1 November 2002, Pages 564-570
Journal home page for Trends in Neurosciences

Review
Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance

https://doi.org/10.1016/S0166-2236(02)02269-5Get rights and content

Abstract

Activity-dependent long-term changes in synaptic efficacy are thought to be important in learning, memory formation, neuronal development and pathological states of neuronal excitability in the CNS. For the past two decades, numerous studies have investigated long-term changes in synaptic efficacy at excitatory glutamatergic synapses. Although inhibitory synapses are essential for proper functioning of the neuronal network, attention has focused only recently on describing and characterizing plasticity at these types of synapse. Not surprisingly, different forms of plasticity at GABAergic, and the closely related glycinergic, synapses have been reported in several regions of the brain. Here we review these different forms of plasticity and focus on their possible roles in developing and adult neuronal networks.

Section snippets

GABAergic and glycinergic synapses undergo long-term plasticity

In the past decade, LTP and LTD of inhibitory synapses have been reported to occur in several regions of the brain, including the hippocampus 5., 6., 7., 8., 9., 10., 11., 12., cortex 13., 14., 15., 16., cerebellum 17., 18., 19., deep cerebellar nucleus 20., 21., 22., lateral superior olive 23., 24. and brain stem 25., 26. (Table 1). LTP of glycinergic synapses that impinge on the Mauthner cells has also been reported to occur in goldfish 27., 28., 29.. Long-term plasticity has been observed on

Long-term plasticity and behavioural repercussion

Because GABAergic interneurons are involved in the induction and maintenance of behaviourally relevant network oscillations in the adult brain 4., 39., one can speculate that long-term plasticity will alter the generation of such rhythms and lead to behavioural modifications. At present, there is no direct evidence in favour of this hypothesis. However, a recent study carried out in the locust olfactory system has shown that synaptic inhibition can change over the course of repeated odour

Conclusion

For a long time, inhibitory synapses have been considered to be important in setting the threshold for synaptic changes at excitatory synapses. The data reviewed here indicate that inhibitory synapses themselves undergo long-term plasticity in different regions of the brain. Not surprisingly, several different mechanisms have been reported to contribute to the induction and persistence of these types of synapse. But, in common with plasticity at excitatory synapses, all forms of plasticity at

Acknowledgements

We thank J. Epsztein and C. Bernard for comments on the manuscript.

References (63)

  • C. Lüscher

    Synaptic plasticity and dynamic modulation of the postsynaptic membrane

    Nat. Neurosci.

    (2000)
  • T. Freund et al.

    Interneurons of the hippocampus

    Hippocampus

    (1996)
  • A. Stelzer

    Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield

    Proc. Natl. Acad. Sci. U. S. A.

    (1994)
  • J.H. Wang et al.

    Shared calcium signalling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites

    J. Neurophysiol.

    (1996)
  • H.A. McLean

    Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus

    J. Physiol. (Lond.)

    (1996)
  • O. Caillard

    Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus

    J. Physiol. (Lond.)

    (1999)
  • O. Caillard

    Mechanisms of induction and expression of long-term depression at GABAergic synapses in neonatal rat hippocampus

    J. Neurosci.

    (1999)
  • O. Caillard

    Activation of presynaptic and postsynaptic ryanodine-sensitive calcium stores is required for the induction of long-term depression at GABAergic synapses in the neonatal rat hippocampus

    J. Neurosci.

    (2000)
  • P. Gubellini

    Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus

    Eur. J. Neurosci.

    (2001)
  • Y. Komatsu et al.

    Long-term modification of inhibitory synaptic transmission in developing visual cortex

    NeuroReport

    (1993)
  • Y. Komatsu

    Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex

    J. Neurosci.

    (1994)
  • Y. Komatsu

    GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate-induced Ca2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses

    J. Neurosci.

    (1996)
  • C.D. Holmgren et al.

    Coincident spiking activity induced long-term changes in inhibition of neocortical pyramidal cells

    J. Neurosci.

    (2001)
  • M. Kano

    Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells

    Nature

    (1992)
  • M. Kano

    Ca2+-induced rebound potentiation of γ-aminobutyric acid-mediated currents requires activation of Ca2+/calmodulin-dependent kinase II

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • T. Hashimoto

    Release of Ca2+ is the crucial step for the potentiation of IPSCs in the cultured cerebellar Purkinje cells of the rat

    J. Physiol. (Lond.)

    (1997)
  • M. Ouardouz et al.

    Mechanisms underlying LTP of inhibitory synaptic transmission in the deep cerebellar nuclei

    J. Neurophysiol.

    (2000)
  • V.C. Kotak et al.

    Long-lasting inhibitory synaptic depression is age- and calcium-dependent

    J. Neurosci.

    (2000)
  • V.C. Kotak

    GABAB and Trk receptor signaling mediates long-lasting inhibitory synaptic depression

    J. Neurophysiol.

    (2001)
  • S.R. Glaum et al.

    Tetanus-induced sustained potentiation of monosynaptic inhibitory transmission in the rat medulla: evidence for a presynaptic locus

    J. Neurophysiol.

    (1996)
  • G. Grabauskas et al.

    Potentiation of GABAergic synaptic transmission in the rostral nucleus of the solitary tract

    Neuroscience

    (1999)
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