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The Journal of Neuroscience, October 15, 2000, 20(20):7539-7546

Activity-Dependent Maintenance of Long-Term Potentiation at Visual Cortical Inhibitory Synapses

Yukio Komatsu and Yumiko Yoshimura

Department of Visual Neuroscience, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan

Neural activity producing a transient increase in intracellular Ca²⁺ concentration can induce long-term potentiation (LTP) at visual cortical inhibitory synapses similar to those seen at various excitatory synapses. Here we report that low-frequency neural activity is required to maintain LTP at these inhibitory synapses. Inhibitory responses of layer 5 cells evoked by layer 4 stimulation were studied in developing rat visual cortical slices under a pharmacological blockade of excitatory synaptic transmission using intracellular and whole-cell recording methods. Although LTP induced by high-frequency stimulation (HFS) persisted while test stimulation was applied at 0.1 Hz, it was not maintained in approximately two-thirds of cells after test stimulation was stopped for 30 min. In the rest of the cells, LTP seemed to be maintained by spontaneous presynaptic spikes, because presynaptic inhibitory cells discharged spontaneously in our experimental condition and because LTP was totally abolished by a temporary application of Na⁺ channel blockers. Experiments applying various Ca²⁺ channel blockers and Ca²⁺ chelators after HFS demonstrated that LTP maintenance was mediated by presynaptic Ca²⁺ entries through multiple types of high-threshold Ca²⁺ channels, which activated Ca²⁺-dependent reactions different from those triggering transmitter release. The Ca²⁺ entries associated with action potentials seemed to be regulated by presynaptic K⁺ channels, presumably large-conductance Ca²⁺-activated K⁺ channels, because the application of blockers for these channels facilitated LTP maintenance. In addition, noradrenaline facilitated the maintenance of LTP. These findings demonstrate a new mechanism by which neural activity regulates the continuation and termination of LTP at visual cortical inhibitory synapses.

Key words: long-term potentiation; maintenance; inhibitory synaptic transmission; Ca²⁺ channels; Ca²⁺-activated K⁺ channels; visual cortex

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20207539-08$05.00/0

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