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The Journal of Neuroscience, November 4, 2009, 29(44):13785-13796; doi:10.1523/JNEUROSCI.2390-09.2009

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Behavioral/Systems/Cognitive
From Neurons to Circuits: Linear Estimation of Local Field Potentials

Malte Rasch,^4,5 Nikos K. Logothetis,⁵ and Gabriel Kreiman^1,2,3

¹Department of Ophthalmology and Neuroscience, Children's Hospital Boston, Harvard Medical School, Boston, Massachusetts 02115, ²Center for Brain Science and ³Swartz Center for Theoretical Neuroscience, Harvard University, Cambridge, Massachusetts 02138, ⁴Graz University of Technology, A8010 Graz, Austria, and ⁵Max Planck Institute for Biological Cybernetics, D-72012 Tübingen, Germany

Correspondence should be addressed to Gabriel Kreiman, Children's Hospital, Harvard Medical School, 3 Blackfan Circle, Boston, MA 02115. Email: gabriel.kreiman{at}tch.harvard.edu

Extracellular physiological recordings are typically separated into two frequency bands: local field potentials (LFPs) (a circuit property) and spiking multiunit activity (MUA). Recently, there has been increased interest in LFPs because of their correlation with functional magnetic resonance imaging blood oxygenation level-dependent measurements and the possibility of studying local processing and neuronal synchrony. To further understand the biophysical origin of LFPs, we asked whether it is possible to estimate their time course based on the spiking activity from the same electrode or nearby electrodes. We used "signal estimation theory" to show that a linear filter operation on the activity of one or a few neurons can explain a significant fraction of the LFP time course in the macaque monkey primary visual cortex. The linear filter used to estimate the LFPs had a stereotypical shape characterized by a sharp downstroke at negative time lags and a slower positive upstroke for positive time lags. The filter was similar across different neocortical regions and behavioral conditions, including spontaneous activity and visual stimulation. The estimations had a spatial resolution of 1 mm and a temporal resolution of 200 ms. By considering a causal filter, we observed a temporal asymmetry such that the positive time lags in the filter contributed more to the LFP estimation than the negative time lags. Additionally, we showed that spikes occurring within 10 ms of spikes from nearby neurons yielded better estimation accuracies than nonsynchronous spikes. In summary, our results suggest that at least some circuit-level local properties of the field potentials can be predicted from the activity of one or a few neurons.

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Received May 21, 2009; revised Aug. 17, 2009; accepted Sept. 11, 2009.

Correspondence should be addressed to Gabriel Kreiman, Children's Hospital, Harvard Medical School, 3 Blackfan Circle, Boston, MA 02115. Email: gabriel.kreiman{at}tch.harvard.edu

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