Correlation of Synaptic Inputs in the Visual Cortex of Awake, Behaving Mice

Highlights

• Vm correlations in V1 depend on behavioral state but not tuning similarity

• Visual stimulation reduces low-frequency and generates high-frequency Vm coherence

• Inhibition lags excitation by ∼5 ms during correlated Vm fluctuations

• Neurons activate in a conserved sequence across stimulus and behavioral states

Summary

The subthreshold mechanisms that underlie neuronal correlations in awake animals are poorly understood. Here, we perform dual whole-cell recordings in the visual cortex (V1) of awake mice to investigate membrane potential (Vm) correlations between upper-layer sensory neurons. We find that the membrane potentials of neighboring neurons display large, correlated fluctuations during quiet wakefulness, including pairs of cells with disparate tuning properties. These fluctuations are driven by correlated barrages of excitation followed closely by inhibition (∼5-ms lag). During visual stimulation, low-frequency activity is diminished, and coherent high-frequency oscillations appear, even for non-preferred stimuli. These oscillations are generated by alternating excitatory and inhibitory inputs at a similar lag. The temporal sequence of depolarization for pairs of neurons is conserved during both spontaneous- and visually-evoked activity, suggesting a stereotyped flow of activation that may function to produce temporally precise “windows of opportunity” for additional synaptic inputs.