Differentiation and Characterization of Excitatory and Inhibitory Synapses by Cryo-electron Tomography and Correlative Microscopy
Open accessAbstract
As key functional units in neural circuits, different types of neuronal synapses play distinct roles in brain information processing, learning, and memory. Synaptic abnormalities are believed to underlie various neurological and psychiatric disorders. Here, by combining cryo-electron tomography and cryo-correlative light and electron microscopy, we distinguished intact excitatory and inhibitory synapses of cultured hippocampal neurons, and visualized the in situ 3D organization of synaptic organelles and macromolecules in their native state. Quantitative analyses of >100 synaptic tomograms reveal that excitatory synapses contain a mesh-like postsynaptic density (PSD) with thickness ranging from 20 to 50 nm. In contrast, the PSD in inhibitory synapses assumes a thin sheet-like structure ∼12 nm from the postsynaptic membrane. On the presynaptic side, spherical synaptic vesicles (SVs) of 25–60 nm diameter and discus-shaped ellipsoidal SVs of various sizes coexist in both synaptic types, with more ellipsoidal ones in inhibitory synapses. High-resolution tomograms obtained using a Volta phase plate and electron filtering and counting reveal glutamate receptor-like and GABA A receptor-like structures that interact with putative scaffolding and adhesion molecules, reflecting details of receptor anchoring and PSD organization. These results provide an updated view of the ultrastructure of excitatory and inhibitory synapses, and demonstrate the potential of our approach to gain insight into the organizational principles of cellular architecture underlying distinct synaptic functions. SIGNIFICANCE STATEMENT To understand functional properties of neuronal synapses, it is desirable to analyze their structure at molecular resolution. We have developed an integrative approach combining cryo-electron tomography and correlative fluorescence microscopy to visualize 3D ultrastructural features of intact excitatory and inhibitory synapses in their native state. Our approach shows that inhibitory synapses contain uniform thin sheet-like postsynaptic densities (PSDs), while excitatory synapses contain previously known mesh-like PSDs. We discovered “discus-shaped” ellipsoidal synaptic vesicles, and their distributions along with regular spherical vesicles in synaptic types are characterized. High-resolution tomograms further allowed identification of putative neurotransmitter receptors and their heterogeneous interaction with synaptic scaffolding proteins. The specificity and resolution of our approach enables precise in situ analysis of ultrastructural organization underlying distinct synaptic functions.
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In vertebrate EM datasets, human annotators can see differences in the vesicles for excitatory and inhibitory synapses.
“In vertebrate EM datasets, human annotators can see differences in the vesicles for excitatory and inhibitory synapses.16,35,36,37,109,110”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [36]
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A cryo-ET survey of microtubules and intracellular compartments in mammalian axons
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Demixing is a default process for biological condensates formed via phase separation
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Synaptic Vesicle Recycling and the Endolysosomal System: A Reappraisal of Form and Function
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Munc13- and SNAP25-dependent molecular bridges play a key role in synaptic vesicle priming
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Monitoring protein communities and their responses to therapeutics
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Rapid and Gentle Immunopurification of Brain Synaptic Vesicles
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Considerations of Antibody Geometric Constraints on NK Cell Antibody Dependent Cellular Cytotoxicity
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Self-citationStructural Analysis of Retrovirus Assembly and Maturation
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Self-citationQuantitative Cryo-Electron Tomography
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The Decade of Super-Resolution Microscopy of the Presynapse
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Guiding the Patterned Growth of Neuronal Axons and Dendrites Using Anisotropic Micropillar Scaffolds
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Mitochondria-ER Tethering in Neurodegenerative Diseases
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Fractional occupancy of synaptic binding sites and the molecular plasticity of inhibitory synapses
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Structural insights into the contactin 1 – neurofascin 155 adhesion complex
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Shanks — multidomain molecular scaffolds of the postsynaptic density
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Analytical Techniques: Shedding Light upon Nanometer-Sized Secretory Vesicles
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Nanomachinery Organizing Release at Neuronal and Ribbon Synapses
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Arrangement of Excitatory Synaptic Inputs on Dendrites of the Medial Superior Olive
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Postsynaptic Proteins at Excitatory Synapses in the Brain—Relationship with Depressive Disorders
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The Nanoscopic Organization of Synapse Structures: A Common Basis for Cell Communication
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The postsynaptic density in excitatory synapses is composed of clustered, heterogeneous nanoblocks
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Self-citationGasdermin D in peripheral nerves: the pyroptotic microenvironment inhibits nerve regeneration
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Complement drives circuit modulation in the adult brain
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SynapseNet: Deep learning for automatic synapse reconstruction
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Structural properties and peptide ligand binding of the capsid homology domains of human Arc
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AMPA receptors in the synapse: Very little space and even less time
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A Survey on Spiking Neural Networks
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Self-citationNeurons as a model system for cryo-electron tomography
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Genetic Probe for Visualizing Glutamatergic Synapses and Vesicles by 3D Electron Microscopy
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Structural basis for noradrenergic regulation of neural circuits in the mouse olfactory bulb
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CryoVesNet: A dedicated framework for synaptic vesicle segmentation in cryo-electron tomograms
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Handling Difficult Cryo-ET Samples: A Study with Primary Neurons from Drosophila melanogaster
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Gephyrin filaments represent the molecular basis of inhibitory postsynaptic densities
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- Authors
- Tao, C.-L., Liu, Y.-T., Sun, R., Zhang, B., Qi, L., Shivakoti, S., Tian, C.-L., Zhang, P., Lau, P.-M., Zhou, Z. H., & Bi, G.-Q.
- Affiliations
- Chinese Academy of Sciences (CN)
- Centre for Human Genetics (GB)
- California NanoSystems Institute (US)
- University of Science and Technology of China (CN)
- Corresponding author
- Zhou, Z. Hong
- Bi, Guo-Qiang
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-01-08
- Volume
- 38
- Issue
- 6
- Pages
- 1493-1510
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5815350
- OpenAlex
- W2783481291
- Cited by
- 207
- References
- 91
- Citations by year
- 2026: 18 · 2025: 24 · 2024: 30 · 2023: 14 · 2022: 27 · 2021: 40 · 2020: 30 · 2019: 17 · 2018: 5 · 2016: 1 · 2012: 1
- FWCI
- 10.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Wellcome Trust (206422/Z/17/Z)
- National Natural Science Foundation of China (2009CB941300, 31070935, PSD-95)
- National Institutes of Health (1s10od018111-01)
- Biotechnology and Biological Sciences Research Council (BB/S003339/1)
- National Institute of General Medical Sciences (R01GM071940)
- National Center for Research Resources (S10RR023057)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- excitatory synapses, inhibitory synapses, synaptic ultrastructure, postsynaptic density, synaptic vesicles, glutamate receptors, GABAA receptor, synaptic scaffolding proteins, adhesion molecules, hippocampal neurons, cryo-electron tomography, correlative light and electron microscopy
- MeSH terms
- Animals, Female, Image Processing, Computer-Assisted, Inhibition, Psychological, Neurons, Pregnancy, Receptors, GABA-A, Synapses, Synaptic Vesicles, Tomography, Cell Adhesion Molecules, Receptors, Glutamate, Excitatory Postsynaptic Potentials, Cryoelectron Microscopy, Rats, Post-Synaptic Density
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