Response Properties of Local Field Potentials and Neighboring Single Neurons in Awake Primary Visual Cortex

Recordings from local field potentials (LFPs) are becoming increasingly common in research and clinical applications, but we still have a poor understanding of how LFP stimulus selectivity originates from the combined activity of single neurons. Here, we systematically compared the stimulus selectivity of LFP and neighboring single-unit activity (SUA) recorded in area primary visual cortex (V1) of awake primates. We demonstrate that LFP and SUA have similar stimulus preferences for orientation, direction of motion, contrast, size, temporal frequency, and even spatial phase. However, the average SUA had 50 times better signal-to-noise, 20% higher contrast sensitivity, 45% higher direction selectivity, and 15% more tuning depth than the average LFP. Low LFP frequencies (<30 Hz) were most strongly correlated with the spiking frequencies of neurons with nonlinear spatial summation and poor orientation/direction selectivity that were located near cortical current sinks (negative LFPs). In contrast, LFP gamma frequencies (>30 Hz) were correlated with a more diverse group of neurons located near cortical sources (positive LFPs). In summary, our results indicate that low- and high-frequency LFP pool signals from V1 neurons with similar stimulus preferences but different response properties and cortical depths.