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The Journal of Neuroscience, May 28, 2008, 28(22):5696-5709; doi:10.1523/JNEUROSCI.0009-08.2008

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Behavioral/Systems/Cognitive
Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information

Andrei Belitski,^1 * Arthur Gretton,^1 * Cesare Magri,^2,3 * Yusuke Murayama,¹ Marcelo A. Montemurro,⁴ Nikos K. Logothetis,^1,5 and Stefano Panzeri^2,4

¹Max Planck Institute for Biological Cybernetics, D-72076 Tübingen, Germany, ²Italian Institute of Technology, Robotics, Brain and Cognitive Sciences Department, I-16163 Genoa, Italy, ³Dipartimento di Informatica e Comunicazione, Università degli Studi di Milano, I-20135 Milan, Italy, ⁴ Faculty of Life Sciences, University of Manchester, Manchester M60 1QD, United Kingdom, and ⁵Imaging Science and Biomedical Engineering, University of Manchester, Manchester M13 9PT, United Kingdom

Correspondence should be addressed to either of the following: Stefano Panzeri, Italian Institute of Technology, Robotics, Brain and Cognitive Sciences Department, via Morego, 30, I-16163 Genoa, Italy, Email: stefano.panzeri{at}iit.it; or Nikos K. Logothetis, Max Planck Institute for Biological Cybernetics, Spemannstrasse 38, D-72076 Tübingen, Germany, E-mail: Email: nikos.logothetis{at}tuebingen.mpg.de

Local field potentials (LFPs) reflect subthreshold integrative processes that complement spike train measures. However, little is yet known about the differences between how LFPs and spikes encode rich naturalistic sensory stimuli. We addressed this question by recording LFPs and spikes from the primary visual cortex of anesthetized macaques while presenting a color movie. We then determined how the power of LFPs and spikes at different frequencies represents the visual features in the movie. We found that the most informative LFP frequency ranges were 1–8 and 60–100 Hz. LFPs in the range of 12–40 Hz carried little information about the stimulus, and may primarily reflect neuromodulatory inputs. Spike power was informative only at frequencies <12 Hz. We further quantified "signal correlations" (correlations in the trial-averaged power response to different stimuli) and "noise correlations" (trial-by-trial correlations in the fluctuations around the average) of LFPs and spikes recorded from the same electrode. We found positive signal correlation between high-gamma LFPs (60–100 Hz) and spikes, as well as strong positive signal correlation within high-gamma LFPs, suggesting that high-gamma LFPs and spikes are generated within the same network. LFPs <24 Hz shared strong positive noise correlations, indicating that they are influenced by a common source, such as a diffuse neuromodulatory input. LFPs <40 Hz showed very little signal and noise correlations with LFPs >40 Hz and with spikes, suggesting that low-frequency LFPs reflect neural processes that in natural conditions are fully decoupled from those giving rise to spikes and to high-gamma LFPs.

Key words: local field potential; macaque; neural coding; V1; movie; multiunit activity

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Received Aug. 22, 2007; revised March 13, 2008; accepted April 16, 2008.

Correspondence should be addressed to either of the following: Stefano Panzeri, Italian Institute of Technology, Robotics, Brain and Cognitive Sciences Department, via Morego, 30, I-16163 Genoa, Italy, Email: stefano.panzeri{at}iit.it; or Nikos K. Logothetis, Max Planck Institute for Biological Cybernetics, Spemannstrasse 38, D-72076 Tübingen, Germany, E-mail: Email: nikos.logothetis{at}tuebingen.mpg.de

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