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Human memory strength is predicted by theta-frequency phase-locking of single neurons

Abstract

Learning from novel experiences is a major task of the central nervous system. In mammals, the medial temporal lobe is crucial for this rapid form of learning1. The modification of synapses and neuronal circuits through plasticity is thought to underlie memory formation2. The induction of synaptic plasticity is favoured by coordinated action-potential timing across populations of neurons3. Such coordinated activity of neural populations can give rise to oscillations of different frequencies, recorded in local field potentials. Brain oscillations in the theta frequency range (3–8 Hz) are often associated with the favourable induction of synaptic plasticity as well as behavioural memory4. Here we report the activity of single neurons recorded together with the local field potential in humans engaged in a learning task. We show that successful memory formation in humans is predicted by a tight coordination of spike timing with the local theta oscillation. More stereotyped spiking predicts better memory, as indicated by higher retrieval confidence reported by subjects. These findings provide a link between the known modulation of theta oscillations by many memory-modulating behaviours and circuit mechanisms of plasticity.

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Figure 1: Task, behavioural results and single-neuron example.
Figure 2: Relationship between spikes and the theta oscillation (3–8 Hz) in the LFP.
Figure 3: The SFC distinguishes between learning trials that were later remembered and those that were forgotten.
Figure 4: SFC time course and relationship to subject confidence.

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Acknowledgements

We thank all patients for their participation; the staff of the Huntington Memorial Hospital epilepsy unit; C. Heller, L. Philpot and W. Sutherling for their support; and F. Mormann, G. Laurent and R. Adolphs for discussion. Funding was provided by the Gordon and Betty Moore Foundation, the William T. Gimbel Discovery Fund and the Howard Hughes Medical Institute.

Author Contributions U.R. designed and performed experiments, wrote analysis methods, analysed data and wrote the paper; A.N.M. and I.B.R. performed surgery; A.N.M. designed experiments; E.M.S. designed experiments and wrote the paper. All authors discussed the results.

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Correspondence to Erin M. Schuman.

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This file contains Supplementary Figures S1-S12 with legends, Supplementary Table 1, a Supplementary Discussion and Supplementary References. (PDF 1529 kb)

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Rutishauser, U., Ross, I., Mamelak, A. et al. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907 (2010). https://doi.org/10.1038/nature08860

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