Neurotrophins and activity-dependent plasticity of cortical interneurons

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Abstract

Neocortical and hippocampal GABA-containing interneurons are susceptible to activity-dependent modulation, such as regulation of soma size, numbers of synaptic contacts, and levels of GABA or neuropeptide expression. In vitro, the effects of neuronal activity on morphology and gene expression of GABA-containing neurons are mimicked, in part, by members of the neurotrophin gene family, such as brain-derived neurotrophic factor (BDNF). In the neocortex and hippocampus, BDNF is synthesized and secreted in an activity-dependent manner by pyramidal neurons, the target cells of GABA-containing neurons, suggesting that BDNF is an activity-dependent, target-derived trophic factor for these interneurons. In support of this, neuronal activity fails to upregulate the expression of neuropeptide Y in hippocampal cultures from BDNF-deficient mice. We, therefore, hypothesize that neurotrophins might mediate some of the actions of neuronal activity on GABA-containing neurons.

Section snippets

Activity-dependent plasticity of GABA-containing neurons

In their classic study on activity-dependent modulation of GABA-containing neurons, Hendry and Jones demonstrated that monocular deprivation (MD) of adult monkeys profoundly modifies the expression pattern of GABA and glutamic acid decarboxylase in the primary visual cortex4, 26. Within five days after removal of one eye, a dramatic downregulation of GABA immunoreactivity was observed, which was most prominent in layers IV A and C. In these layers the thalamic afferents arising from different

Neurotrophins as differentiation factors for GABA-containing neurons

Besides neuronal activity, growth factors are likely to play an important role in regulating the level of expression of GABA, Ca2+-binding proteins or neuropeptides, and the morphology of GABA-containing neurons. In particular, members of the neurotrophin gene family, namely BDNF, NT-3 and NT-4/5 ([34]), have been shown to promote the neurochemical and morphological differentiation of various groups of hippocampal and neocortical GABA-containing neurons. For example, NT-3 stimulates the

BDNF as an activity-dependent regulated, target-derived trophic factor for GABA-containing neurons

The recognition that the synthesis and the secretion of BDNF and NGF are regulated by electrical activity raises the interesting possibility that neurotrophins are involved in the activity-dependent plasticity of the nervous system21, 22, 23, 24, 25, 40, 41, 42. Substantial evidence is accumulating showing that neurotrophins might influence the activity-dependent development of cortical connectivity. The treatment with chimeric molecules consisting of the extracellular domain of the BDNF

Acute modulation of GABAergic transmission by neurotrophins

In addition to the long-term effects on the morphological and neurochemical characteristics of GABA-containing neurons described above, neurotrophins might also contribute to the activity-dependent regulation of GABAergic function by acutely modulating transmission at GABA-containing synapses. Neurotrophins have been shown to regulate cholinergic or glutamatergic transmission within a few minutes, involving both pre- and postsynaptic mechanisms[61]. Recent studies indicate that acute modulation

Acknowledgements

We thank Hans Thoenen for his strong commitment to our research work, and his helpful criticisms of the manuscript. We are also grateful to Jonathan Cooper and Alexander Rabchevsky for critical reading of the manuscript. We thank Kristina D. Micheva and Clermont Beaulieu for their kind permission to reproduce a figure from their original study ([29]). SM is supported by a grant from Fondation pour le Recherche Médicale and BB by a long-term research fellowship from the Human Frontier Science

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