Directed and acyclic synaptic connectivity in the human layer 2-3 cortical microcircuit

Author:

Peng Yangfan1ORCID,Bjelde Antje1ORCID,Aceituno Pau Vilimelis2ORCID,Mittermaier Franz X.1ORCID,Planert Henrike1ORCID,Grosser Sabine3ORCID,Onken Julia4,Faust Katharina4ORCID,Kalbhenn Thilo5ORCID,Simon Matthias5ORCID,Radbruch Helena6ORCID,Fidzinski Pawel78ORCID,Schmitz Dietmar89ORCID,Alle Henrik1ORCID,Holtkamp Martin10ORCID,Vida Imre3ORCID,Grewe Benjamin F.2ORCID,Geiger Jörg R. P.1ORCID

Affiliation:

1. Institute of Neurophysiology, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

2. Institute of Neuroinformatics, University of Zurich and ETH Zurich, 8057 Zürich, Switzerland.

3. Institute for Integrative Neuroanatomy, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

4. Department of Neurosurgery, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

5. Department of Neurosurgery (Evangelisches Klinikum Bethel), Medical School, Bielefeld University, 33617 Bielefeld, Germany.

6. Department of Neuropathology, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

7. Clinical Study Center, Berlin Institute of Health at Charité–Universitätsmedizin Berlin, 10117 Berlin, Germany.

8. German Center for Neurodegenerative Diseases (DZNE) Berlin, 10117 Berlin, Germany.

9. Neuroscience Research Center, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

10. Epilepsy-Center Berlin-Brandenburg, Department of Neurology, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin, 10117 Berlin, Germany.

Abstract

The computational capabilities of neuronal networks are fundamentally constrained by their specific connectivity. Previous studies of cortical connectivity have mostly been carried out in rodents; whether the principles established therein also apply to the evolutionarily expanded human cortex is unclear. We studied network properties within the human temporal cortex using samples obtained from brain surgery. We analyzed multineuron patch-clamp recordings in layer 2-3 pyramidal neurons and identified substantial differences compared with rodents. Reciprocity showed random distribution, synaptic strength was independent from connection probability, and connectivity of the supragranular temporal cortex followed a directed and mostly acyclic graph topology. Application of these principles in neuronal models increased dimensionality of network dynamics, suggesting a critical role for cortical computation.

Publisher

American Association for the Advancement of Science (AAAS)

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