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The Journal of Neuroscience, February 15, 2002, 22(4):1328-1337
Activity Deprivation Reduces Miniature IPSC Amplitude by
Decreasing the Number of Postsynaptic GABAA Receptors
Clustered at Neocortical Synapses
Valerie
Kilman,
Mark C. W.
van
Rossum, and
Gina G.
Turrigiano
Department of Biology and Center for Complex Systems, Brandeis
University, Waltham, Massachusetts 02454
Maintaining the proper balance between excitation and inhibition is
necessary to prevent cortical circuits from either falling silent or
generating epileptiform activity. One mechanism through which cortical
networks maintain this balance is through the activity-dependent regulation of inhibition, but whether this is achieved primarily through changes in synapse number or synaptic strength is not clear.
Previously, we found that 2 d of activity deprivation increased the amplitude of miniature EPSCs (mEPSCs) onto cultured visual cortical pyramidal neurons. Here we find that this same manipulation decreases the amplitude of mIPSCs. This occurs with no change in
single-channel conductance but is accompanied by a reduction in the
average number of channels open during the mIPSC peak and a reduction
in the intensity of staining for GABAA receptors
(GABAARs) at postsynaptic sites. In addition, the number of
synaptic sites that express detectable levels of GABAARs
was decreased by ~50% after activity blockade, although there was no
reduction in the total number of presynaptic contacts. These data
suggest that activity deprivation reduces cortical inhibition by
reducing both the number of GABAARs clustered at synaptic
sites and the number of functional inhibitory synapses. Because
excitatory and inhibitory synaptic currents are regulated in opposite
directions by activity blockade, these data suggest that the balance
between excitation and inhibition is dynamically regulated by ongoing activity.
Key words:
synaptic plasticity; activity-dependent; mIPSC; GABAA receptor; synapse elimination; nonstationary
fluctuation analysis
Copyright © 2002 Society for Neuroscience 0270-6474/02/2241328-10$05.00/0
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[Full Text]
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|