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Hippocampal–cortical interaction during periods of subcortical silence

Abstract

Hippocampal ripples, episodic high-frequency field-potential oscillations primarily occurring during sleep and calmness, have been described in mice, rats, rabbits, monkeys and humans, and so far they have been associated with retention of previously acquired awake experience. Although hippocampal ripples have been studied in detail using neurophysiological methods, the global effects of ripples on the entire brain remain elusive, primarily owing to a lack of methodologies permitting concurrent hippocampal recordings and whole-brain activity mapping. By combining electrophysiological recordings in hippocampus with ripple-triggered functional magnetic resonance imaging, here we show that most of the cerebral cortex is selectively activated during the ripples, whereas most diencephalic, midbrain and brainstem regions are strongly and consistently inhibited. Analysis of regional temporal response patterns indicates that thalamic activity suppression precedes the hippocampal population burst, which itself is temporally bounded by massive activations of association and primary cortical areas. These findings suggest that during off-line memory consolidation, synergistic thalamocortical activity may be orchestrating a privileged interaction state between hippocampus and cortex by silencing the output of subcortical centres involved in sensory processing or potentially mediating procedural learning. Such a mechanism would cause minimal interference, enabling consolidation of hippocampus-dependent memory.

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Figure 1: Sharp wave–ripple complexes.
Figure 2: Examples of ripple-triggered BOLD maps in anaesthetized and awake monkeys.
Figure 3: Average ripple-triggered maps, signal dynamics and activation fractions.
Figure 4: Gamma-triggered population BOLD responses.
Figure 5: BOLD response dynamics.
Figure 6: Resting-state fMRI.

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Acknowledgements

We thank D. Omer and M. Munk for reading the manuscript and for useful suggestions, D. Blaurock for English language corrections and editing, and P. Douay for help with the alert monkey experiments. This research was supported by the Max Planck Society. We apologize to those whose work we have not been able to cite for reasons of space.

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Authors and Affiliations

Authors

Contributions

N.K.L and O.E. designed the experiments and carried out research. N.K.L. analysed the data, wrote the manuscript and supervised the research. Y.M. carried out research and, together with M.B., contributed data analysis. M.A. and T.S. collected the physiology fMRI data, H.C.E. helped with all anatomical details required to define ROIs and enable three-dimensional registration of functional images to standard anatomical scans, and A.O. designed and developed all electronics and electrodes permitting concurrent multiple-contact electrophysiological recordings and fMRI.

Corresponding author

Correspondence to N. K. Logothetis.

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The authors declare no competing financial interests.

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Logothetis, N., Eschenko, O., Murayama, Y. et al. Hippocampal–cortical interaction during periods of subcortical silence. Nature 491, 547–553 (2012). https://doi.org/10.1038/nature11618

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