Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Balakrishnan, Veeramuthu; Puthussery, Theresa; Kim, Mean Hwan; Taylor, W. Rowland; Gersdorff, Henrique von

doi:10.1016/j.neuron.2015.07.016

Cited by 31 publications

(70 citation statements)

References 74 publications

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“…This tighter VGCC arrangement presumably allows for more efficient coupling between Ca 2+ entry and SV release at 4 wk compared with 2 wk and is consistent with the finding that the blocking efficiency of EGTA on transmitter release decreases with age at the calyx of Held (34, 52, 53; review: ref. 16), at PF-PC synapses (32), and at amacrine cell synapses (54). Likewise, recent morphological data show an age-dependent tightening of the VGCC-SV arrangement in AZs of the fly neuromuscular junction (23).…”

Section: Discussionmentioning

confidence: 85%

Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Miki

Kaufmann

Malagón

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

107

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Many central synapses contain a single presynaptic active zone and a single postsynaptic density. Vesicular release statistics at such "simple synapses" indicate that they contain a small complement of docking sites where vesicles repetitively dock and fuse. In this work, we investigate functional and morphological aspects of docking sites at simple synapses made between cerebellar parallel fibers and molecular layer interneurons. Using immunogold labeling of SDS-treated freeze-fracture replicas, we find that Ca v 2.1 channels form several clusters per active zone with about nine channels per cluster. The mean value and range of intersynaptic variation are similar for Ca v 2.1 cluster numbers and for functional estimates of docking-site numbers obtained from the maximum numbers of released vesicles per action potential. Both numbers grow in relation with synaptic size and decrease by a similar extent with age between 2 wk and 4 wk postnatal. Thus, the mean docking-site numbers were 3.15 at 2 wk (range: 1-10) and 2.03 at 4 wk (range: 1-4), whereas the mean numbers of Ca v 2.1 clusters were 2.84 at 2 wk (range: 1-8) and 2.37 at 4 wk (range: 1-5). These changes were accompanied by decreases of miniature current amplitude (from 93 pA to 56 pA), active-zone surface area (from 0.0427 μm 2 to 0.0234 μm 2 ), and initial success rate (from 0.609 to 0.353), indicating a tightening of synaptic transmission with development. Altogether, these results suggest a close correspondence between the number of functionally defined vesicular docking sites and that of clusters of voltage-gated calcium channels.neurotransmitter release | active zone | calcium channel | release site | parallel fiber I n presynaptic terminals, the active zone (AZ) represents a highly specialized structure allowing the binding and Ca 2+ -dependent release of synaptic vesicles (SVs) (1). Fluctuation analysis of synaptic signals suggests the presence of one or several functional units per AZ (2, 3). These units are either called "release sites" or "docking sites," and their number per AZ represents the maximum SV output that this structure can provide per action potential (AP). In recent years, optical methods have been developed to record single-SV release (4). Notably, studies using superresolution and total internal reflection fluorescence imaging in functioning central synapses have provided information on the kinetics (5) and subsynaptic localization (6) of single-SV docking and release. Despite these advances, electrophysiological methods remain the most rapid and sensitive method to assess SV exocytosis at central synapses such as the calyx of Held (7) or cerebellar mossy fiber terminals (8). In recent years, electrophysiological recordings performed at special synapses containing a single AZ and a single postsynaptic density (PSD), called "simple synapses," revealed a fixed maximum in the number of SVs that can be released per AZ by a short calcium stimulus (9-11), providing a direct evaluation of the number of docking sites per AZ. This number ran...

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Section: Discussionmentioning

confidence: 85%

Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Miki

Kaufmann

Malagón

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

107

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“…Prominent targets of CaBPs, including CaBP1 and CaBP2, are the voltage-gated Ca 2+ channels (Lee et al, 2002; Haeseleer et al, 2004; Zhou et al, 2004; Cui et al, 2007; Rieke et al, 2008; Schrauwen et al, 2012). Voltage-gated Ca 2+ channels are directly involved in vesicle exocytosis and are a possible target for CaBP1/CD and CaBP2 in bipolar cells and amacrine cells (Pan et al, 2001; Habermann et al, 2003; Singer and Diamond, 2003; Balakrishnan et al, 2015). Specifically for CaBP1, it was shown that CaBP1 has opposite effects depending on the type of voltage-gated Ca 2+ channels it modulates (Haeseleer et al, 2000; Lee et al, 2002; Zhou et al, 2004; Cui et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Lack of CaBP1/Caldendrin or CaBP2 Leads to Altered Ganglion Cell Responses

Sinha

Lee

Haeseleer

2016

eNeuro

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“…Ames medium was used for recordings from mouse retinal slices (see Balakrishnan et al, 2015). Whole-cell voltage-clamp recordings were obtained with an EPC-9 double amplifier (HEKA Electronik) using 7–12 MΩ pipettes with Cs-based internal solutions.…”

Section: Methodsmentioning

confidence: 99%

Postsynaptic Plasticity Triggered by Ca2+-Permeable AMPA Receptor Activation in Retinal Amacrine Cells

Kim

Gersdorff

2016

Neuron

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SUMMARY Amacrine cells are thought to be a major locus for mechanisms of light adaptation and contrast enhancement in the retina. However, the potential for plasticity in their AMPA receptor currents remains largely unknown. Using paired patch-clamp recordings between bipolar cell terminals and amacrine cells, we have simultaneously measured presynaptic membrane capacitance changes and EPSCs. Repetitive bipolar cell depolarizations, designed to maintain the same amount of exocytosis, nevertheless significantly potentiated evoked EPSCs in a subpopulation of amacrine cells. Likewise, repetitive iontophoresis (or puffs) of glutamate (or AMPA) onto the dendrites of amacrine cells also significantly potentiated evoked currents and [Ca2+]i rises. However, strong postsynaptic Ca2+ buffering with BAPTA abolished the potentiation and selective antagonists of Ca2+-permeable AMPA receptors also blocked the potentiation of AMPA-mediated currents. Together these results suggest that Ca2+ influx via Ca2+-permeable AMPA receptors can elicit a rapid form of postsynaptic plasticity in a subgroup of amacrine cell dendrites.

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Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Cited by 31 publications

References 74 publications

Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Lack of CaBP1/Caldendrin or CaBP2 Leads to Altered Ganglion Cell Responses

Postsynaptic Plasticity Triggered by Ca2+-Permeable AMPA Receptor Activation in Retinal Amacrine Cells

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Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Cited by 31 publications

References 74 publications

Numbers of presynaptic Ca 2+ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Numbers of presynaptic Ca 2+ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Lack of CaBP1/Caldendrin or CaBP2 Leads to Altered Ganglion Cell Responses

Postsynaptic Plasticity Triggered by Ca2+-Permeable AMPA Receptor Activation in Retinal Amacrine Cells

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Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses

Numbers of presynaptic Ca ²⁺ channel clusters match those of functionally defined vesicular docking sites in single central synapses