Synaptic Integration in Rat Frontal Cortex Shaped by Network Activity

TLDR

Neocortical neurons in vivo operate within highly active networks, yet the impact of this activity on their integrative properties remains largely unknown, a gap because most knowledge comes from in vitro studies with diminished network activity. The study aims to determine how varying levels of network activity affect synaptic integration in rat frontal cortex. Using intracellular recordings in anesthetized rat frontal cortex, the authors measured the relationship between membrane potential excursions and surrounding network spiking, and examined how input summation varies across different membrane potential states and network activity levels. They found that synaptic integration remains linear regardless of network activity, but high activity markedly reduces response amplitude and duration, shortening the temporal integration window and demanding tighter presynaptic coordination, underscoring the importance of neuronal cooperation in the active brain.

Abstract

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.