Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Hook, Matthew J. Van; Parmelee, Caitlyn; Chen, Ming‐Hui; Cork, Karlene M.; Curto, Carina; Thoreson, Wallace B.

doi:10.1085/jgp.201411229

Cited by 29 publications

(36 citation statements)

References 113 publications

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“…2010; Van Hook et al. 2014). When the amplitude of the fast component of EPSC charge transfer was scaled by the number of ribbon contacts measured from the EPSC peak amplitude (36 pA/ribbon) this gave a mean IRP amplitude of 383 ± 25 fC/ribbon ( n = 24) or 25 ± 2 vesicles/ribbon (15.5 fC/vesicle) (Cadetti et al.…”

Section: Resultsmentioning

confidence: 99%

“…2010b; Van Hook et al. 2014). Endogenous levels of Ca 2+ buffering might be able to support sustained synaptic transmission by cones by enhancing Ca 2+ /CaM-dependent acceleration of replenishment.…”

Section: Resultsmentioning

confidence: 99%

“…2010a; Van Hook et al. 2014). With the transition from –39 to –19 mV, the slope of the cumulative charge transfer steepens, indicative of enhanced CaM-dependent replenishment from increased Ca 2+ influx (Babai et al.…”

Section: Resultsmentioning

confidence: 99%

“…2010a; Van Hook et al. 2014). Ca 2+ acting through calmodulin (CaM) accelerates this resupply process by acting on ribbon-associated proteins to enhance the likelihood of vesicle attachment (Van Hook et al.…”

Section: Introductionmentioning

confidence: 99%

“…Ca 2+ acting through calmodulin (CaM) accelerates this resupply process by acting on ribbon-associated proteins to enhance the likelihood of vesicle attachment (Van Hook et al. 2014). One question posed in this study is whether the mechanisms regulating sustained and transient release of vesicles from ribbons are similar in rods and cones.…”

Section: Introductionmentioning

confidence: 99%

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Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

Hook

Thoreson

2015

Physiol Rep

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Differences in synaptic transmission between rod and cone photoreceptors contribute to different response kinetics in rod- versus cone-dominated visual pathways. We examined Ca2+ dynamics in synaptic terminals of tiger salamander photoreceptors under conditions that mimicked endogenous buffering to determine the influence on kinetically and mechanistically distinct components of synaptic transmission. Measurements of ICl(Ca) confirmed that endogenous Ca2+ buffering is equivalent to ˜0.05 mmol/L EGTA in rod and cone terminals. Confocal imaging showed that with such buffering, depolarization stimulated large, spatially unconstrained [Ca2+] increases that spread throughout photoreceptor terminals. We calculated immediately releasable pool (IRP) size and release efficiency in rods by deconvolving excitatory postsynaptic currents and presynaptic Ca2+ currents. Peak efficiency of ˜0.2 vesicles/channel was similar to that of cones (˜0.3 vesicles/channel). Efficiency in both cell types was not significantly affected by using weak endogenous Ca2+ buffering. However, weak Ca2+ buffering speeded Ca2+/calmodulin (CaM)-dependent replenishment of vesicles to ribbons in both rods and cones, thereby enhancing sustained release. In rods, weak Ca2+ buffering also amplified sustained release by enhancing CICR and CICR-stimulated release of vesicles at nonribbon sites. By contrast, elevating [Ca2+] at nonribbon sites in cones with weak Ca2+ buffering and by inhibiting Ca2+ extrusion did not trigger additional release, consistent with the notion that exocytosis from cones occurs exclusively at ribbons. The presence of weak endogenous Ca2+ buffering in rods and cones facilitates slow, sustained exocytosis by enhancing Ca2+/CaM-dependent replenishment of ribbons in both rods and cones and by stimulating nonribbon release triggered by CICR in rods.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

Hook

Thoreson

2015

Physiol Rep

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The role of PDLIM1, a PDZ‐LIM domain protein, at the ribbon synapses in the chicken retina

Rı́os

Paganelli

Fosser

2020

J of Comparative Neurology

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PDLIM's protein family is involved in the rearrangement of the actin cytoskeleton. In the present study, we describe the localization of PDLIM1 in chicken photoreceptors.This study provides evidence that this protein is present at the cone pedicles, as well as in other synapses of the chicken retina. Here, we demonstrate the expression pattern of PDLIM1 through immunofluorescence staining, immunoblots, subcellular fractionation, and immunoprecipitation experiments. Also, we consider the possibility that PDLIM1 may be involved in the synaptic vesicle endocytosis and/or the presynaptic trafficking of synaptic vesicles back to the nonready releasable pool. This endocytotic/exocytotic coupling requires a tight link between exocytic vesicle fusion at defined release sites and endocytic retrieval of synaptic vesicle membranes. In turn, photoreceptor ribbon synaptic structure depends on the cytoskeleton arrangement, both at the active zone-related with exocytosis-as well as at the endocytic zoneperiactive zone. To our knowledge, the PDLIM1 protein has not been observed in the pre synapses of the retina. Thus, the present study describes the expression and subcellular localization of PDLIM1 for the first time, as well as its modulation by visual environment in the chicken retina. K E Y W O R D SPDLIM1, PDZ and Lim protein 1, photoreceptors, retina, ribbon synapses, RRID:

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Modeling and measurement of vesicle pools at the cone ribbon synapse: Changes in release probability are solely responsible for voltage‐dependent changes in release

Thoreson

Hook

Parmelee

et al. 2015

Synapse

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Post-synaptic responses are a product of quantal amplitude (Q), size of the releasable vesicle pool (N), and release probability (P). Voltage-dependent changes in presynaptic Ca2+ entry alter post-synaptic responses primarily by changing P but have also been shown to influence N. With simultaneous whole cell recordings from cone photoreceptors and horizontal cells in tiger salamander retinal slices, we measured N and P at cone ribbon synapses by using a train of depolarizing pulses to stimulate release and deplete the pool. We developed an analytical model that calculates the total pool size contributing to release under different stimulus conditions by taking into account the prior history of release and empirically-determined properties of replenishment. The model provided a formula that calculates vesicle pool size from measurements of the initial post-synaptic response and limiting rate of release evoked by a train of pulses, the fraction of release sites available for replenishment, and the time constant for replenishment. Results of the model showed that weak and strong depolarizing stimuli evoked release with differing probabilities but the same size vesicle pool. Enhancing intraterminal Ca2+ spread by lowering Ca2+ buffering or applying BayK8644 did not increase PSCs evoked with strong test steps showing there is a fixed upper limit to pool size. Together, these results suggest that light-evoked changes in cone membrane potential alter synaptic release solely by changing release probability.

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Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Abstract: Calmodulin promotes vesicle replenishment at photoreceptor ribbon synapses, enabling cones to transmit higher-frequency visual information.

Cited by 29 publications

References 113 publications

Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

The role of PDLIM1, a PDZ‐LIM domain protein, at the ribbon synapses in the chicken retina

Modeling and measurement of vesicle pools at the cone ribbon synapse: Changes in release probability are solely responsible for voltage‐dependent changes in release

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Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Abstract: Calmodulin promotes vesicle replenishment at photoreceptor ribbon synapses, enabling cones to transmit higher-frequency visual information.

Cited by 29 publications

References 113 publications

Weak endogenous Ca2+buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

Weak endogenous Ca2+buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

The role of PDLIM1, a PDZ‐LIM domain protein, at the ribbon synapses in the chicken retina

Modeling and measurement of vesicle pools at the cone ribbon synapse: Changes in release probability are solely responsible for voltage‐dependent changes in release

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Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina

Weak endogenous Ca²⁺buffering supports sustained synaptic transmission by distinct mechanisms in rod and cone photoreceptors in salamander retina