The extracellular matrix molecule brevican is an integral component of the machinery mediating fast synaptic transmission at the calyx of Held
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Key points: The proteoglycan brevican is a major component of the extracellular matrix of perineuronal nets and is highly enriched in the perisynaptic space suggesting a role for synaptic transmission. We have introduced the calyx of Held in the auditory brainstem as a model system to study the impact of brevican on dynamics and reliability of synaptic transmission. In vivo extracellular single‐unit recordings at the calyx of Held in brevican‐deficient mice yielded a significant increase in the action potential (AP) transmission delay and a prolongation of pre‐ and postsynaptic APs. The changes in dynamics of signal transmission were accompanied by the reduction of presynaptic vGlut1 and ultrastructural changes in the perisynaptic space. These data show that brevican is an important mediator of fast synaptic transmission at the calyx of Held. The extracellular matrix is an integral part of the neural tissue. Its most conspicuous manifestation in the brain are the perineuronal nets (PNs) which surround somata and proximal dendrites of distinct neuron types. The chondroitin sulfate proteoglycan brevican is a major component of PNs. In contrast to other PN‐comprising proteoglycans (e.g. aggrecan and neurocan), brevican is mainly expressed in the perisynaptic space closely associated with both the pre‐ and postsynaptic membrane. This specific localization prompted the hypothesis that brevican might play a role in synaptic transmission. In the present study we specifically investigated the role of brevican in synaptic transmission at a central synapse, the calyx of Held in the medial nucleus of the trapezoid body, by the use of in vivo electrophysiology, immunohistochemistry, biochemistry and electron microscopy. In vivo extracellular single‐unit recordings were acquired in brevican‐deficient mice and the dynamics and reliability of synaptic transmission were compared to wild‐type littermates. In knockout mice, the speed of pre‐to‐postsynaptic action potential (AP) transmission was reduced and the duration of the respective pre‐ and postsynaptic APs increased. The reliability of signal transmission, however, was not affected by the lack of brevican. The changes in dynamics of signal transmission were accompanied by the reduction of (i) presynaptic vGlut1 and (ii) the size of subsynaptic cavities. The present results suggest an essential role of brevican for the functionality of high‐speed synaptic transmission at the calyx of Held.
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Brevican affects mainly excitatory synapses, regulating both AMPA receptors and potassium channels and the speed and duration of synaptic potentials, leading to impaired hippocampal LTP observed in brevican knockout animals.
“For example, brevican affects mainly excitatory synapses, regulating both AMPA receptors and potassium channels and the speed and duration of synaptic potentials, leading to impaired hippocampal LTP observed in brevican knockout animals [34, 65, 72].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [72]
The Introduction (page not supplied) reports slower transmission and prolonged action potentials at the excitatory calyx of Held synapse in brevican-knockout mice. The Discussion (page not supplied) reports disturbed hippocampal LTP maintenance, but not impaired initiation. It proposes, rather than establishes, effects on AMPA receptors and potassium-channel activity; it found no change in their measured expression and does not establish that brevican affects mainly excitatory synapses. (LLM, conf=0.88)
Experimental — accuracy not yet measuredKnockout of brevican slows pre-to-postsynaptic action potential transmission and prolongs pre- and postsynaptic potentials.
“The CSPG brevican is enriched in the perisynaptic space of the Calyx, and knockout of brevican slows pre-to-postsynaptic action potential transmission and prolongs pre-and postsynaptic potentials [72].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [72]
Structural modification of perineuronal nets alters synaptic transmission, synapse number, and the ion channel/neurotransmitter receptor composition of synapses.
“the structural modification of PNNs alters synaptic transmission [27], synapse number [28], and the ion channel/neurotransmitter receptor composition of synapses [29]”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [27]
In brainstem auditory nuclei of mice, genetic loss of brevican contributes to loss of brevican-expressing PNNs.
“In brainstem auditory nuclei of mice, genetic loss of brevican contributes to loss of brevican-expressing PNNs”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Blosa et al., 2015
In brainstem auditory nuclei of mice, genetic loss of brevican contributes to reduced sound-evoked firing rates.
“as well as reduced sound-evoked firing rates”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Blosa et al., 2015
In brainstem auditory nuclei of mice, genetic loss of brevican contributes to increased neuronal response thresholds.
“and increased neuronal response thresholds (Blosa et al., 2015).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Blosa et al., 2015
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- Authors
- Blosa, M., Sonntag, M., Jäger, C., Weigel, S., Seeger, J., Frischknecht, R., Seidenbecher, C. I., Matthews, R. T., Arendt, T., Rübsamen, R., & Morawski, M.
- Affiliations
- Leipzig University (DE)
- Leibniz Institute for Neurobiology (DE)
- SUNY Upstate Medical University (US)
- Corresponding author
- Morawski, Markus
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2015-08-30
- Volume
- 593
- Issue
- 19
- Pages
- 4341-4360
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC4594243
- OpenAlex
- W1546509016
- Cited by
- 74
- References
- 83
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 3 · 2023: 3 · 2022: 9 · 2021: 14 · 2020: 10 · 2019: 6 · 2018: 10 · 2017: 7 · 2016: 4
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (Mo2249/2-1, Ru390/20-1)
- EU-COST Action BM1001 (11861)
- European Union and the Federal State of Saxony
- Schram foundation (T287/21796/2011)
- German Research Foundation (GRK1167)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- brevican, calyx of Held, perineuronal nets, extracellular matrix, fast synaptic transmission, VGLUT1, medial nucleus of the trapezoid body, auditory brainstem, proteoglycans
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Extracellular Matrix, Female, Male, Mice, Inbred C57BL, Synaptic Transmission, Synapses, Mice, Knockout, Excitatory Amino Acid Transporter 2, Glucose Transporter Type 1, Glucose Transporter Type 2, Mice, Brevican, Trapezoid Body
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