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

doi:10.1016/j.celrep.2023.112397

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

Cell Rep. 2023 May 30;42(5):112397. doi: 10.1016/j.celrep.2023.112397. Epub 2023 Apr 18.

Authors

Mark Rigby¹, Federico W Grillo¹, Benjamin Compans¹, Guilherme Neves², Julia Gallinaro³, Sophie Nashashibi¹, Sally Horton¹, Pedro M Pereira Machado⁴, Maria Alejandra Carbajal⁴, Gema Vizcay-Barrena⁴, Florian Levet⁵, Jean-Baptiste Sibarita⁶, Angus Kirkland⁷, Roland A Fleck⁴, Claudia Clopath³, Juan Burrone⁸

Affiliations

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: juan.burrone@kcl.ac.uk.

Abstract

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.

Keywords: CP: Neuroscience; axon; connectome; dendrite; hippocampus; multi-synaptic bouton; network synchrony; synapse.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Dendrites
Hippocampus*
Neurons
Presynaptic Terminals*
Synapses

Abstract

Publication types

MeSH terms

Grants and funding