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The Journal of Neuroscience, February 25, 2004, 24(8):1839-1851; doi:10.1523/JNEUROSCI.3500-03.2004

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Behavioral/Systems/Cognitive
Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons

Lucinda A. Grande,³ Gregory A. Kinney,² Greta L. Miracle,³ and William J. Spain^1,3

Departments of ¹Physiology and Biophysics, Neurology, and ²Rehabilitation Medicine, University of Washington, Seattle, Washington 98105, and ³Veterans Affairs Puget Sound Health Care System, Seattle, Washington 98108

The firing rate of neocortical pyramidal neurons is believed to represent primarily the average arrival rate of synaptic inputs; however, it has also been found to vary somewhat depending on the degree of synchrony among synaptic inputs. We investigated the ability of pyramidal neurons to perform coincidence detection, that is, to represent input timing in their firing rate, and explored some factors that influence that representation. We injected computer-generated simulated synaptic inputs into pyramidal neurons during whole-cell recordings, systematically altering the phase delay between two groups of periodic simulated input events. We explored how input intensity, the synaptic time course, inhibitory synaptic conductance, and input jitter influenced the firing rate representation of input timing. In agreement with computer modeling studies, we found that input synchronization increases firing rate when intensity is low but reduces firing rate when intensity is high. At high intensity, the effect of synchrony on firing rate could be switched from reducing to increasing firing rate by shortening the simulated excitatory synaptic time course, adding inhibition (using the dynamic clamp technique), or introducing a small input jitter. These opposite effects of synchrony may serve different computational functions: as a means of increasing firing rate it may be useful for efficient recruitment or for computing a continuous parameter, whereas as a means of decreasing firing rate it may provide gain control, which would allow redundant or excessive input to be ignored. Modulation of dynamic input properties may allow neurons to perform different operations depending on the task at hand.

Key words: coincidence detection; synchrony; phase delay; neocortex; pyramidal neuron; synaptic inhibition; jitter; dynamic clamp

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Received July 26, 2003; revised December 5, 2003; accepted December 30, 2003.

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