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
Affiliations
Mark Rigby
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
Federico W. Grillo
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
Benjamin Compans
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
Guilherme Neves
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
Julia Gallinaro
Bioengineering Department, Imperial College London, London, UK
Sophie Nashashibi
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
Sally Horton
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
Pedro M. Pereira Machado
Centre for Ultrastructural Imaging (CUI), Kings College London, New Hunts House, Guys Hospital Campus, London SE1 1UL, UK
Maria Alejandra Carbajal
Centre for Ultrastructural Imaging (CUI), Kings College London, New Hunts House, Guys Hospital Campus, London SE1 1UL, UK
Gema Vizcay-Barrena
Centre for Ultrastructural Imaging (CUI), Kings College London, New Hunts House, Guys Hospital Campus, London SE1 1UL, UK
Florian Levet
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
Jean-Baptiste Sibarita
University Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297, 33000 Bordeaux, France
Angus Kirkland
The Rosalind Franklin Institute, Harwell Campus, Didcot OX11 0FA, UK
Roland A. Fleck
Centre for Ultrastructural Imaging (CUI), Kings College London, New Hunts House, Guys Hospital Campus, London SE1 1UL, UK
Claudia Clopath
Bioengineering Department, Imperial College London, London, UK
Juan Burrone
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; Corresponding author
Summary: 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.
