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1 Neurobiology, Yale University School of Medicine, New Haven, Connecticut, United States; Kavli Institute for Neuroscience, New Haven, Connecticut, United States
2 Neurobiology, Yale University School of Medicine, New Havan, Connecticut, United States; Kavli Institute for Neuroscience, New Haven, Connecticut, United States
3 Neurobiology, Yale University School of Medicine, New Havan, Connecticut, United States; Kavli Institute for Neuroscience, New Haven, Connecticut, United States; Crick-Jacobs Center for Theoretical and Computational Biology, The Salk Institute for Biological Studies, La Jolla, California, United States
* To whom correspondence should be addressed. E-mail: david.mccormick{at}yale.edu.
Spontaneous activity within local circuits affects the integrative properties of neurons and networks. We have previously demonstrated that neocortical network activity exhibits a balance between excitatory and inhibitory synaptic potentials, and such activity has significant effects upon synaptic transmission, action potential generation, and spike timing. However, whether such activity facilitates or reduces sensory responses has yet to be clearly determined. We examined this hypothesis in the primary visual cortex in vivo, during slow oscillations in ketamine-xylazine anesthetized cats. We measured network activity (Up states) with extracellular recording, while simultaneously recording post-synaptic potentials (PSPs) and action potentials in nearby cells. Stimulating the receptive field revealed that spiking responses of both simple and complex cells were significantly enhanced (more than two-fold) during network activity, as were spiking responses to intracellular injection of varying amplitude artificial conductance stimuli. Visually evoked PSPs were not significantly different in amplitude during network activity or quiescence; instead, spontaneous depolarization caused by network activity brought these evoked PSPs closer to firing threshold. Further examination revealed that visual responsiveness was gradually enhanced by progressive membrane potential depolarization. These spontaneous depolarizations enhanced responsiveness to stimuli of varying contrasts, resulting in an upward (multiplicative) scaling of the contrast response function. Our results suggest that small increases in ongoing balanced network activity that result in depolarization may provide a rapid and generalized mechanism to control the responsiveness (gain) of cortical neurons, such as occurs during shifts in spatial attention.
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