Multi-synaptic boutons are a feature of CA1 hippocampal connections in the stratum oriens

Mark Rigby, Federico W. Grillo, Benjamin Compans, Guilherme Neves, Julia Gallinaro, Sophie Nashashibi, Sally Horton, Pedro M. Pereira Machado, Maria Alejandra Carbajal, Gema Vizcay-Barrena, Florian Levet, Jean-Baptiste Sibarita, Angus Kirkland, Roland A. Fleck, Claudia Clopath, Juan Burrone
Cell Reports. 2023-05-01; 42(5): 112397
DOI: 10.1016/j.celrep.2023.112397

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Rigby M(1), Grillo FW(1), Compans B(1), Neves G(2), Gallinaro J(3), Nashashibi
S(1), Horton S(1), Pereira Machado PM(4), Carbajal MA(4), Vizcay-Barrena G(4),
Levet F(5), Sibarita JB(6), Kirkland A(7), Fleck RA(4), Clopath C(3), Burrone
J(8).

Author information:
(1)MRC Centre for Neurodevelopmental Disorders, Institute of Psychiatry,
Psychology and Neuroscience, King’s College London, London SE1 1UL, UK; Centre
for Developmental Neurobiology, Institute of Psychiatry, Psychology and
Neuroscience, King’s College London, London SE1 1UL, UK.
(2)MRC Centre for Neurodevelopmental Disorders, Institute of Psychiatry,
Psychology and Neuroscience, King’s College London, London SE1 1UL, UK; Centre
for Developmental Neurobiology, Institute of Psychiatry, Psychology and
Neuroscience, King’s College London, London SE1 1UL, UK; The Rosalind Franklin
Institute, Harwell Campus, Didcot OX11 0FA, UK.
(3)Bioengineering Department, Imperial College London, London, UK.
(4)Centre for Ultrastructural Imaging (CUI), Kings College London, New Hunts
House, Guys Hospital Campus, London SE1 1UL, UK.
(5)University Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience,
IINS, UMR 5297, 33000 Bordeaux, France; University Bordeaux, CNRS, INSERM,
Bordeaux Imaging Center, BIC, UAR3420, US 4, 33000 Bordeaux, France.
(6)University Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience,
IINS, UMR 5297, 33000 Bordeaux, France.
(7)The Rosalind Franklin Institute, Harwell Campus, Didcot OX11 0FA, UK.
(8)MRC Centre for Neurodevelopmental Disorders, Institute of Psychiatry,
Psychology and Neuroscience, King’s College London, London SE1 1UL, UK; Centre
for Developmental Neurobiology, Institute of Psychiatry, Psychology and
Neuroscience, King’s College London, London SE1 1UL, UK. Electronic address:
.

Excitatory synapses are typically described as single synaptic boutons (SSBs),
where one presynaptic bouton contacts a single postsynaptic spine. Using serial
section block-face scanning electron microscopy, we found that this textbook
definition of the synapse does not fully apply to the CA1 region of the
hippocampus. Roughly half of all excitatory synapses in the stratum oriens
involved multi-synaptic boutons (MSBs), where a single presynaptic bouton
containing multiple active zones contacted many postsynaptic spines (from 2 to
7) on the basal dendrites of different cells. The fraction of MSBs increased
during development (from postnatal day 22 [P22] to P100) and decreased with
distance from the soma. Curiously, synaptic properties such as active zone (AZ)
or postsynaptic density (PSD) size exhibited less within-MSB variation when
compared with neighboring SSBs, features that were confirmed by super-resolution
light microscopy. Computer simulations suggest that these properties favor
synchronous activity in CA1 networks.

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

DOI: 10.1016/j.celrep.2023.112397
PMCID: PMC10695768
PMID: 37074915 [Indexed for MEDLINE]

Conflict of interest statement: Declaration of interests The authors declare no
competing interests.

Auteurs Bordeaux Neurocampus