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Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex

Abstract

Animal studies have shown robust electrophysiological activity in the sensory cortex in the absence of stimuli or tasks. Similarly, recent human functional magnetic resonance imaging (fMRI) revealed widespread, spontaneously emerging cortical fluctuations. However, it is unknown what neuronal dynamics underlie this spontaneous activity in the human brain. Here we studied this issue by combining bilateral single-unit, local field potentials (LFPs) and intracranial electrocorticography (ECoG) recordings in individuals undergoing clinical monitoring. We found slow (<0.1 Hz, following 1/f-like profiles) spontaneous fluctuations of neuronal activity with significant interhemispheric correlations. These fluctuations were evident mainly in neuronal firing rates and in gamma (40–100 Hz) LFP power modulations. Notably, the interhemispheric correlations were enhanced during rapid eye movement and stage 2 sleep. Multiple intracranial ECoG recordings revealed clear selectivity for functional networks in the spontaneous gamma LFP power modulations. Our results point to slow spontaneous modulations in firing rate and gamma LFP as the likely correlates of spontaneous fMRI fluctuations in the human sensory cortex.

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Figure 1: Two models of possible neuronal activity underlying fMRI events.
Figure 2: Interhemispheric comparison of slow spontaneous activity in human auditory cortex.
Figure 3: Profiles of correlated spontaneous activity.
Figure 4: Cross- and autocorrelograms.
Figure 5: Firing-rate and ISI distributions during rest and stimulation.
Figure 6: Spatial topography of spontaneous correlations in intracranial ECoG data.

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Acknowledgements

We thank the participants for volunteering to take part in the study; A.D. Ekstrom, E. Isham, E. Ho, T.A. Fields, and E. Behnke for technical assistance at UCLA; C. Wilson and J. Ogren for help with sleep recordings and staging; D. Yossef, S. Nagar, R. Cohen, C. Yosef, G. Yehezkel and the EEG technicians for assistance at the Tel Aviv Medical Center; and R. Paz and E. Schneidman for helpful discussions and feedback. This study was funded by the Israel Science Foundation, Minerva and Benoziyo Center grants to R. Malach, a US-Israel Binational Science Foundation grant to I.F. and R. Malach and a Human Frontier Science Program Organization fellowship to R. Mukamel.

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Correspondence to Rafael Malach.

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Nir, Y., Mukamel, R., Dinstein, I. et al. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11, 1100–1108 (2008). https://doi.org/10.1038/nn.2177

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