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The Journal of Neuroscience, November 12, 2003, 23(32):10388-10401
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Cellular/Molecular
Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons
Yousheng Shu,1 * Andrea Hasenstaub,1 * Mathilde Badoual,2 Thierry Bal,2 andDavid A. McCormick1 1Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510, and 2Integrative and Computational Neurosciences Unit, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2191, Institut de Neurobiologie Alfred Fessard 1, 91198 Gif-sur-Yvette Cedex, France
Ongoing synaptic activity, ever present in cortical neurons, may vary widely in its amplitude and characteristics, potentially having a strong influence on neuronal processing. Intracellular recordings in layer 5 pyramidal cells in prefrontal and visual cortical slices maintained in vitro revealed spontaneous periods of synaptic bombardment. Testing the responsiveness of these cortical cells to synaptic inputs or the injection of artificial excitatory postsynaptic conductances of various amplitudes revealed that background synaptic activity dramatically increased the probability of response to small inputs, decreased the slope of the input-output curve, and decreased both the latency and jitter of action potential activation. Examining the effects of different components of synaptic barrages (namely, depolarization, increase in membrane conductance, and increase in membrane potential variance) revealed that the effects observed were dominated by the membrane depolarization and increase in variance. Depolarization increased the peak cross-correlation between injected complex in vivo-like waveforms through enhancement of responsiveness to small inputs, whereas increases in variance did so through a shift in firing mode from one of threshold detection to probabilistic discharge. These results indicate that rapid increases in neuronal responsiveness, as well as increases in spike timing precision, can be achieved through balanced barrages of excitatory and inhibitory synaptic activity.
Key words: cortex; gain; responsiveness; synaptic activity; multiplication; timing
Received June 12, 2003; revised June 12, 2003; accepted September 17, 2003.
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