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Strong and reliable synaptic communication between pyramidal neurons in adult human cerebral cortex

2022; Oxford University Press; Volume: 33; Issue: 6 Linguagem: Inglês

10.1093/cercor/bhac246

1460-2199

Sarah Hunt, Yoni Leibner, Eline J. Mertens, Natalí Barros-Zulaica, Lida Kanari, Tim S. Heistek, Mahesh M. Karnani, Romy Aardse, René Wilbers, Djai B. Heyer, Natalia A. Goriounova, Matthijs B Verhoog, Guilherme Testa-Silva, Joshua Obermayer, Tamara Versluis, Ruth Benavides‐Piccione, Philip de Witt-Hamer, Sander Idema, David P. Noske, Johannes C. Baayen, Ed S. Lein, Javier DeFelipe, Henry Markram, Huibert D. Mansvelder, Felix Schürmann, Idan Segev, Christiaan P. J. de Kock,

EEG and Brain-Computer Interfaces

Abstract Synaptic transmission constitutes the primary mode of communication between neurons. It is extensively studied in rodent but not human neocortex. We characterized synaptic transmission between pyramidal neurons in layers 2 and 3 using neurosurgically resected human middle temporal gyrus (MTG, Brodmann area 21), which is part of the distributed language circuitry. We find that local connectivity is comparable with mouse layer 2/3 connections in the anatomical homologue (temporal association area), but synaptic connections in human are 3-fold stronger and more reliable (0% vs 25% failure rates, respectively). We developed a theoretical approach to quantify properties of spinous synapses showing that synaptic conductance and voltage change in human dendritic spines are 3–4-folds larger compared with mouse, leading to significant NMDA receptor activation in human unitary connections. This model prediction was validated experimentally by showing that NMDA receptor activation increases the amplitude and prolongs decay of unitary excitatory postsynaptic potentials in human but not in mouse connections. Since NMDA-dependent recurrent excitation facilitates persistent activity (supporting working memory), our data uncovers cortical microcircuit properties in human that may contribute to language processing in MTG.