Encoding Light Intensity by the Cone Photoreceptor Synapse

Choi, Sue-Yeon; Borghuis, Bart G.; Rea, Ruth; Levitan, Edwin S.; Sterling, Peter; Krämer, Richard

doi:10.1016/j.neuron.2005.09.011

Cited by 71 publications

(90 citation statements)

References 46 publications

(67 reference statements)

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“…(b) Glutamate refilling of vesicles exhibits a time constant of 15 s (Hori and Takahashi, 2012), far slower than the fast component of replenishment ( 800 ms). The reason that glutamate refilling does not normally become rate limiting is likely because of the large cytosolic reservoir pool that provides a substantial buffer of previously loaded vesicles; salamander cones contain 194,000 vesicles (Choi et al, 2005), with 85% participating in vesicle cycling (Rea et al, 2004;M. Chen et al, 2013).…”

Section: Mechanisms Of Cam Effects On Replenishmentmentioning

confidence: 99%

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

Hook¹,

Parmelee²,

Chen³

et al. 2014

J Cell Biol

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At the first synapse in the vertebrate visual pathway, light-evoked changes in photoreceptor membrane potential alter the rate of glutamate release onto second-order retinal neurons. This process depends on the synaptic ribbon, a specialized structure found at various sensory synapses, to provide a supply of primed vesicles for release. Calcium (Ca 2+ ) accelerates the replenishment of vesicles at cone ribbon synapses, but the mechanisms underlying this acceleration and its functional implications for vision are unknown. We studied vesicle replenishment using paired whole-cell recordings of cones and postsynaptic neurons in tiger salamander retinas and found that it involves two kinetic mechanisms, the faster of which was diminished by calmodulin (CaM) inhibitors. We developed an analytical model that can be applied to both conventional and ribbon synapses and showed that vesicle resupply is limited by a simple time constant,  = 1/(Ds), where D is the vesicle diffusion coefficient,  is the vesicle diameter,  is the vesicle density, and s is the probability of vesicle attachment. The combination of electrophysiological measurements, modeling, and total internal reflection fluorescence microscopy of single synaptic vesicles suggested that CaM speeds replenishment by enhancing vesicle attachment to the ribbon. Using electroretinogram and whole-cell recordings of light responses, we found that enhanced replenishment improves the ability of cone synapses to signal darkness after brief flashes of light and enhances the amplitude of responses to higherfrequency stimuli. By accelerating the resupply of vesicles to the ribbon, CaM extends the temporal range of synaptic transmission, allowing cones to transmit higher-frequency visual information to downstream neurons. Thus, the ability of the visual system to encode time-varying stimuli is shaped by the dynamics of vesicle replenishment at photoreceptor synaptic ribbons.

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Section: Mechanisms Of Cam Effects On Replenishmentmentioning

confidence: 99%

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

Hook¹,

Parmelee²,

Chen³

et al. 2014

J Cell Biol

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“…Procedures for FM1-43 loading and unloading were modified from those described previously (Choi et al, 2005a). The retina was mounted onto filter paper and loaded with 30 M FM1-43 (Invitrogen, Eugene, OR) for 2 h and washed with 1 mM Advasep-7 (CyDex, Lenexa, KS) for 10 min.…”

Section: Fm1-43 Dye Loading and Unloadingmentioning

confidence: 99%

“…Gecko and salamander retinas were prepared and fixed for EM as described previously (Rea et al, 2004;Choi et al, 2005a). Vesicle density in photoreceptor terminals was calculated from ultrathin EM sections (70 nm).…”

Section: Electron Microscopymentioning

confidence: 99%

“…We then compared this data with previous measurements of dye release from anole cones (Choi et al, 2005a). Gecko retina is advantageous because the rod terminals are large (5-10 m diameter), facilitating optical measurements from an individual cell, and they are also homogenous, allowing simultaneous fluorescent measurement from an array of terminals in the OPL.…”

Section: Release Of Fm1-43 In the Dark Is Slow In Rodsmentioning

confidence: 99%

“…We previously measured dark release from photoreceptors in the cone-only retina of anole lizards (Choi et al, 2005a). We imaged the loss of the fluorescent synaptic vesicle dye FM1-43 and used electron microscopy (EM) to count synaptic vesicles in the terminals to estimate the vesicle release rate.…”

Section: Introductionmentioning

confidence: 99%

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Synaptic Ca²⁺in Darkness Is Lower in Rods than Cones, Causing Slower Tonic Release of Vesicles

Sheng¹,

Choi²,

Dharia³

et al. 2007

J. Neurosci.

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Rod and cone photoreceptors use specialized biochemistry to generate light responses that differ in their sensitivity and kinetics. However, it is unclear whether there are also synaptic differences that affect the transmission of visual information. Here, we report that in the dark, rods tonically release synaptic vesicles at a much slower rate than cones, as measured by the release of the fluorescent vesicle indicator FM1-43. To determine whether slower release results from a lower Ca 2ϩ sensitivity or a lower dark concentration of Ca 2ϩ , we imaged fluorescent indicators of synaptic vesicle cycling and intraterminal Ca 2ϩ . We report that the Ca 2ϩ sensitivity of release is indistinguishable in rods and cones, consistent with their possessing similar release machinery. However, the dark intraterminal Ca 2ϩ concentration is lower in rods than in cones, as determined by two-photon Ca 2ϩ imaging. The lower level of dark Ca 2ϩ ensures that rods encode intensity with a slower vesicle release rate that is better matched to the lower information content of dim light.

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A Sparse and Spike‐Timing‐Based Adaptive Photoencoder for Augmenting Machine Vision for Spiking Neural Networks

et al. 2022

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The representation of external stimuli in the form of action potentials or spikes constitutes the basis of energy efficient neural computation that emerging spiking neural networks (SNNs) aspire to imitate. With recent evidence suggesting that information in the brain is more often represented by explicit firing times of the neurons rather than mean firing rates, it is imperative to develop novel hardware that can accelerate sparse and spike‐timing‐based encoding. Here a medium‐scale integrated circuit composed of two cascaded three‐stage inverters and one XOR logic gate fabricated using a total of 21 memtransistors based on photosensitive 2D monolayer MoS2 for spike‐timing‐based encoding of visual information, is introduced. It is shown that different illumination intensities can be encoded into sparse spiking with time‐to‐first‐spike representing the illumination information, that is, higher intensities invoke earlier spikes and vice versa. In addition, non‐volatile and analog programmability in the photoencoder is exploited for adaptive photoencoding that allows expedited spiking under scotopic (low‐light) and deferred spiking under photopic (bright‐light) conditions, respectively. Finally, low energy expenditure of less than 1 µJ by the 2D‐memtransistor‐based photoencoder highlights the benefits of in‐sensor and bioinspired design that can be transformative for the acceleration of SNNs.

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Encoding Light Intensity by the Cone Photoreceptor Synapse

Cited by 71 publications

References 46 publications

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

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

Synaptic Ca²⁺in Darkness Is Lower in Rods than Cones, Causing Slower Tonic Release of Vesicles

A Sparse and Spike‐Timing‐Based Adaptive Photoencoder for Augmenting Machine Vision for Spiking Neural Networks

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Encoding Light Intensity by the Cone Photoreceptor Synapse

Cited by 71 publications

References 46 publications

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

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

Synaptic Ca2+in Darkness Is Lower in Rods than Cones, Causing Slower Tonic Release of Vesicles

A Sparse and Spike‐Timing‐Based Adaptive Photoencoder for Augmenting Machine Vision for Spiking Neural Networks

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Synaptic Ca²⁺in Darkness Is Lower in Rods than Cones, Causing Slower Tonic Release of Vesicles