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The Journal of Neuroscience, August 23, 2006, 26(34):8787-8799; doi:10.1523/JNEUROSCI.1792-06.2006

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Behavioral/Systems/Cognitive
Diversity of Gain Modulation by Noise in Neocortical Neurons: Regulation by the Slow Afterhyperpolarization Conductance

Matthew H. Higgs,¹ Sean J. Slee,¹ and William J. Spain^1,2,3

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

Correspondence should be addressed to William J. Spain, Department of Neurology (127), 1660 South Columbian Way, Seattle, WA 98108. Email: spain{at}u.washington.edu

Neuronal firing is known to depend on the variance of synaptic input as well as the mean input current. Several studies suggest that input variance, or "noise," has a divisive effect, reducing the slope or gain of the firing frequency–current (f–I) relationship. We measured the effects of current noise on f–I relationships in pyramidal neurons and fast-spiking (FS) interneurons in slices of rat sensorimotor cortex. In most pyramidal neurons, noise had a multiplicative effect on the steady-state f–I relationship, increasing gain. In contrast, noise reduced gain in FS interneurons. Gain enhancement in pyramidal neurons increased with stimulus duration and was correlated with the amplitude of the slow afterhyperpolarization (sAHP), a major mechanism of spike-frequency adaptation. The 5-HT₂ receptor agonist -methyl-5-HT reduced the sAHP and eliminated gain increases, whereas augmenting the sAHP conductance by spike-triggered dynamic-current clamp enhanced the gain increase. These results indicate that the effects of noise differ fundamentally between classes of neocortical neurons, depending on specific biophysical properties including the sAHP conductance. Thus, noise from background synaptic input may enhance network excitability by increasing gain in pyramidal neurons with large sAHPs and reducing gain in inhibitory FS interneurons.

Key words: noise; gain; pyramidal neuron; interneuron; sAHP; coincidence detection

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Received Nov. 4, 2005; revised July 10, 2006; accepted July 11, 2006.

Correspondence should be addressed to William J. Spain, Department of Neurology (127), 1660 South Columbian Way, Seattle, WA 98108. Email: spain{at}u.washington.edu

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