TY - JOUR
T1 - Strong and reliable synaptic communication between pyramidal neurons in adult human cerebral cortex
AU - Hunt, Sarah
AU - Leibner, Yoni
AU - Mertens, Eline J.
AU - Barros-Zulaica, Natalí
AU - Kanari, Lida
AU - Heistek, Tim S.
AU - Karnani, Mahesh M.
AU - Aardse, Romy
AU - Wilbers, René
AU - Heyer, Djai B.
AU - Goriounova, Natalia A.
AU - Verhoog, Matthijs B.
AU - Testa-Silva, Guilherme
AU - Obermayer, Joshua
AU - Versluis, Tamara
AU - Benavides-Piccione, Ruth
AU - De Witt-Hamer, Philip
AU - Idema, Sander
AU - Noske, David P.
AU - Baayen, Johannes C.
AU - Lein, Ed S.
AU - Defelipe, Javier
AU - Markram, Henry
AU - Mansvelder, Huibert D.
AU - Schürmann, Felix
AU - Segev, Idan
AU - De Kock, Christiaan P.J.
N1 - Publisher Copyright:
© 2022 The Author(s). Published by Oxford University Press. All rights reserved.
PY - 2023/3/15
Y1 - 2023/3/15
N2 - 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.
AB - 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.
KW - cortex
KW - human brain
KW - L2/L3
KW - NMDA receptor
KW - synaptic transmission
UR - http://www.scopus.com/inward/record.url?scp=85138593040&partnerID=8YFLogxK
U2 - 10.1093/cercor/bhac246
DO - 10.1093/cercor/bhac246
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C2 - 35802476
AN - SCOPUS:85138593040
SN - 1047-3211
VL - 33
SP - 2857
EP - 2878
JO - Cerebral Cortex
JF - Cerebral Cortex
IS - 6
ER -