The growth of synaptic endings in the mammalian brain: A study of the calyces of the trapezoid body

Morest, D. Kent

doi:10.1007/bf00526129

Cited by 190 publications

(134 citation statements)

References 18 publications

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“…In addition to the release modality transformation, it is also important to note that the morphological structure of the calyx of Held undergoes a significant transformation from spoon shape to finger digit-like (Morest, 1968;von Gersdorff and Borst, 2002). By P14, the morphological structure of calyces is considered to be fully mature.…”

Section: Discussionmentioning

confidence: 99%

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Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Fedchyshyn¹,

Wang²

2005

J. Neurosci.

264

326

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] o and was independent of postsynaptic receptor desensitization. We demonstrated that release from P8 -P12 terminals involved both N-and P/Q-type VGCCs, but P/Q-type-associated release sites specifically displayed low m values. These results suggest a developmental transformation of the release modality from "microdomain," involving cooperative action of many loosely coupled N-and P/Q-type VGCCs, to "nanodomain," in which opening of fewer tightly coupled P/Q-type VGCCs effectively induce a fusion event. Spatial tightening improves the release efficiency and is likely a critical step for the development of high-fidelity neurotransmission in this and other central synapses.

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Section: Discussionmentioning

confidence: 99%

“…The calyx of Held synapse undergoes dramatic morphological refinement over the first two postnatal weeks (Morest, 1968;von Gersdorff and Borst, 2002). The "spoon-shaped" calyx at early postnatal stages may slow glutamate removal, whereas older "finger-digit-like" terminals allow more rapid clearance of glutamate from the synaptic cleft.…”

Section: Distinctivementioning

confidence: 99%

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Fedchyshyn¹,

Wang²

2005

J. Neurosci.

264

326

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“…The surface area of the calyx increased about fivefold from P8 to P14 and then settled at a twofold larger surface area at P23 compared with P8. An increase of the surface with constant volume suggests that a fissioning process rather than appositional growth underlies the maturation of the calyx from a club-like structure into its digitated adult morphology (Morest, 1968;Kandler and Friauf, 1993). The transient peak in surface area coinciding with the onset of hearing may suggest that activity-dependent synaptic pruning contributes to the adult connectivity in the MNTB.…”

Section: Sequestration Into Distinct Membrane-delimited Compartmentsmentioning

confidence: 99%

“…At postnatal day 5 (P5), calyces are club-shaped and extend several thin filopodia, whereas they form a highly digitated structure in the mature state at around P21 (Morest, 1968;Kandler and Friauf, 1993). These morphological changes are accompanied by distinct changes in the properties of synaptic transmission (von Gersdorff and Borst, 2002).…”

Section: Introductionmentioning

confidence: 99%

Donut-Like Topology of Synaptic Vesicles with a Central Cluster of Mitochondria Wrapped into Membrane Protrusions: A Novel Structure–Function Module of the Adult Calyx of Held

et al. 2006

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Structural and functional properties of synapses are intricately and reciprocally coupled. To cope with the functional requirements in auditory processing, the calyx of Held developed distinct structural specializations such as a large number of active zones, large size, elaborate morphology, and defined distribution of ion channels. These specializations typically appear during postnatal maturation within the first 3 weeks of life and are accompanied by marked changes in the properties of synaptic transmission. We examined the arrangement of synaptic vesicles at different postnatal stages of maturation by genetically labeling vesicles with the fluorescent fusion protein synaptophysin-enhanced green fluorescent protein. Fluorescence and electron microscopy-based analyses revealed a new anatomical specialization in the mature calyx of Held. Within small, membrane-delimited compartments (swellings), synaptic vesicles formed donut-like assemblies around a central cluster of interconnected mitochondria. Adult calyces contained ϳ100 such structural units, each of them consisting of ϳ800 synaptic vesicles, six to nine mitochondria, and five to nine active zones. A donut of synaptic vesicles measured ϳ1 m in diameter and was placed in a swelling with a volume of ϳ5 fl. Conspicuously, this structural specialization appears with the onset of hearing and may contribute to maturational changes in presynaptic function.

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“…Although there are detailed accounts of the morphological changes in this synapse at various postnatal stages (Morest, 1968;Kuwabara et al 1991), much less is known about the functional development of high-fidelity synaptic transmission particularly in mice (Futai et al 2001). We have characterized developmental changes in Toronto,Ontario,Canada M5G 1X8 synaptic properties of the mouse calyx of Held-MNTB synapse within the first three postnatal weeks.…”

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confidence: 99%

Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

Joshi

Wang

2002

J Physiology

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Using whole-cell recordings from presynaptic terminals and postsynaptic principal neurons in the mouse medial nucleus of the trapezoid body (MNTB), we have characterized properties of the calyx of Held synapse during the first three postnatal weeks. We observed that evoked excitatory postsynaptic currents (EPSCs) mediated by NMDA receptors (NMDAR) increased until postnatal day 11/12 (P11/12) after which they declined to very low or undetectable levels at P16. Meanwhile, EPSCs mediated by AMPA receptors (AMPAR) showed an approximate three-fold increase in amplitude. These changes were paralleled by NMDAR and AMPAR currents evoked by exogenous NMDA and kainate to MNTB neurons except that whole-cell kainate currents remained constant after P7/8 while AMPAR-EPSCs continued to increase. We found that the decay time constant t for NMDAR-EPSCs and AMPAR-EPSCs declined by about 30 % and 70 %, respectively. Analyses of NMDAR-EPSCs with subunit-specific pharmacological agents including ifenprodil, N,N,N‚,N‚-tetrakis(2-pyridylmethyl)-ethylenediamine (TPEN), zinc and Mg 2+ revealed subtle developmental changes in subunit composition. As maturation progressed, this synapse displayed a reduction in the number of presynaptic spike failures and the extent of synaptic depression in response to trains of stimuli (50-300 Hz) while the recovery rate from depression accelerated. These results demonstrate profound changes in the size and kinetics of postsynaptic glutamate receptors and in the spike-firing capability of presynaptic terminals at the calyx of Held-MNTB synapse during early development. We suggest that these concurrent presynaptic and postsynaptic adaptations represent important steps for synapse consolidation and refinement and ultimately for the development of fast high-fidelity transmission at this synapse. synaptic properties of the mouse calyx of Held-MNTB synapse within the first three postnatal weeks. We found that synaptic NMDARs were present only transiently within the first 2 weeks, and exhibited a unique developmental profile. Although synaptic AMPARs exhibited a nearly linear growth in density over the same period, the total population of functional AMPARs (i.e. whole-cell kainate currents) reached a maximum by the end of the first postnatal week. We suggest that these changes, along with concurrent alterations in kinetic properties of EPSCs and in synaptic depression and recovery, contribute significantly to the development of high-fidelity synaptic transmission at this synapse. Part of this study had been previously published in abstract form (Joshi & Wang, 2000). METHODS Slice preparationMice were housed in the facility certified by the Canadian Council of Animal Care and used for this study according to a protocol approved by the Hospital for Sick Children Animal Care Committee. Brainstem slices were prepared from P3-P18 mice (CD1/C57 black) as previously described (Forsythe & BarnesDavis, 1993). Mice were decapitated with a small guillotine and brains were rapidly dissected and immersed in ice-cold artif...

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The growth of synaptic endings in the mammalian brain: A study of the calyces of the trapezoid body

Cited by 190 publications

References 18 publications

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Developmental Transformation of the Release Modality at the Calyx of Held Synapse

Donut-Like Topology of Synaptic Vesicles with a Central Cluster of Mitochondria Wrapped into Membrane Protrusions: A Novel Structure–Function Module of the Adult Calyx of Held

Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem

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