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Synaptic Integration in Rat Frontal Cortex Shaped by Network Activity

¹Neurobiology and Biophysics, Department of Biology III, Albert-Ludwigs-University, Freiburg, Germany; ²Laboratoire de Neurobiologie Cellulaire et Moléculaire, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8544, Ecole Normale Supérieure, Paris Cedex, France; ³Department of Neurology, Massachusetts General Hospital, Charlestown, Massachusetts; and ⁴Department of Anatomy and Neurobiology, University of Tennessee, Health Science Center, Memphis, Tennessee

Submitted 24 January 2003; accepted in final form 5 August 2004

Neocortical neurons in vivo are embedded in networks with intensive ongoing activity. How this network activity affects the neurons’ integrative properties and what function this may imply at the network level remain largely unknown. Most of our knowledge regarding synaptic communication and integration is based on recordings in vitro, where network activity is strongly diminished or even absent. Here, we present results from two complementary series of experiments based on intracellular in vivo recordings in anesthetized rat frontal cortex. Specifically, we measured 1) the relationship between the excursions of a neuron’s membrane potential and the spiking activity in the surrounding network and 2) how the summation of several inputs to a single neuron changes with the different levels of its membrane potential excursions and the associated states of network activity. The combination of these measurements enables us to assess how the level of network activity influences synaptic integration. We present direct evidence that integration of synaptic inputs in frontal cortex is linear, independent of the level of network activity. However, during periods of high network activity, the neurons’ response to synaptic input is markedly reduced in both amplitude and duration. This results in a drastic shortening of its window for temporal integration, requiring more precise coordination of presynaptic spike discharges to reliably drive the neuron to spike under conditions of high network activity. We conclude that ongoing activity, as present in the active brain, emphasizes the need for neuronal cooperation at the network level, and cannot be ignored in the exploration of cortical function.

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