Membrane potential states gate synaptic consolidation in human neocortical tissue

Franz X. Mittermaier, Thilo Kalbhenn, Ran Xu, Julia Onken, Katharina Faust, Thomas Sauvigny, Ulrich W. Thomale, Angela M. Kaindl, Martin Holtkamp, Sabine Grosser, Pawel Fidzinski, Matthias Simon, Henrik Alle and Jörg R. P. Geiger ()
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Franz X. Mittermaier: Institute of Neurophysiology
Thilo Kalbhenn: University of Bielefeld Medical Center OWL
Ran Xu: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Julia Onken: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Katharina Faust: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Thomas Sauvigny: University Medical Center Hamburg-Eppendorf
Ulrich W. Thomale: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Angela M. Kaindl: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Martin Holtkamp: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Sabine Grosser: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
Pawel Fidzinski: Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, NeuroCure Cluster of Excellence
Matthias Simon: University of Bielefeld Medical Center OWL
Henrik Alle: Institute of Neurophysiology
Jörg R. P. Geiger: Institute of Neurophysiology

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract Synaptic mechanisms that contribute to human memory consolidation remain largely unexplored. Consolidation critically relies on sleep. During slow wave sleep, neurons exhibit characteristic membrane potential oscillations known as UP and DOWN states. Coupling of memory reactivation to these slow oscillations promotes consolidation, though the underlying mechanisms remain elusive. Here, we performed axonal and multineuron patch-clamp recordings in acute human brain slices, obtained from neurosurgeries, to show that sleep-like UP and DOWN states modulate axonal action potentials and temporarily enhance synaptic transmission between neocortical pyramidal neurons. Synaptic enhancement by UP and DOWN state sequences facilitates recruitment of postsynaptic action potentials, which in turn results in long-term stabilization of synaptic strength. In contrast, synapses undergo lasting depression if presynaptic neurons fail to recruit postsynaptic action potentials. Our study offers a mechanistic explanation for how coupling of neural activity to slow waves can cause synaptic consolidation, with potential implications for brain stimulation strategies targeting memory performance.

Date: 2024
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DOI: 10.1038/s41467-024-53901-2

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