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.2005.12.007

Cited by 14 publications

(19 citation statements)

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“…However, our data show that photoreceptors compress the 4-5 log unit dynamic range obtained by the phototransduction cascade in the OS (Fain et al, 2001) into a 20-fold operating range of [Ca 2+ ]i within the presynaptic terminal. This resembles the 28-fold range for exocytosis in synaptic terminals of cones (Choi et al, 2005) and suggests that photoreceptor output is controlled by Ca 2+ homeostatic mechanisms within the terminal. Thus presynaptic gain control by Ca 2+ extrusion, release from stores (Križaj et al, 1999(Križaj et al, ,2003, neuromodulation (Stella et al, 2002) and feedback from horizontal cells (Verweij et al, 1996;Vessey et al, 2005) may mediate presynaptic adaptation via regulation of terminal [Ca 2+ ].…”

Section: Spatiotemporal Ca 2+ Gradient Within the Photoreceptor Innermentioning

confidence: 59%

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The dynamic range and domain-specific signals of intracellular calcium in photoreceptors

Szikra

Križaj²

2006

Neuroscience

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Vertebrate photoreceptors consist of strictly delimited subcellular domains: the outer segment, ellipsoid, cell body and synaptic terminal, each hosting crucial cellular functions, including phototransduction, oxidative metabolism, gene expression and transmitter release. We used optical imaging to explore the spatiotemporal dynamics of Ca(2+) signaling in non-outer segment regions of rods and cones. Sustained depolarization, designed to emulate photoreceptor activation in the darkness, evoked a standing Ca(2+) gradient in tiger salamander photoreceptors with spatially-averaged intracellular Ca(2+) concentration within synaptic terminals of approximately 2 microM and lower (approximately 750 nM) intracellular calcium concentration in the ellipsoid. Measurements from axotomized cell bodies and isolated ellipsoids showed that Ca(2+) enters the two compartments via both local L-type Ca(2+) channels and diffusion. The results from optical imaging studies were supported by immunostaining analysis. L-type voltage-operated Ca(2+) channels and plasma membrane Ca(2+) ATPases were highly expressed in synaptic terminals with progressively lower expression levels in the cell body and ellipsoid. These results show photoreceptor Ca(2+) homeostasis is controlled in a region-specific manner by direct Ca(2+) entry and diffusion as well as Ca(2+) extrusion. Moreover, quantitative measurement of intracellular calcium concentration levels in different photoreceptor compartments indicates that the dynamic range of Ca(2+) signaling in photoreceptors is approximately 40-fold, from approximately 50 nM in the light to approximately 2 microM in darkness.

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Section: Spatiotemporal Ca 2+ Gradient Within the Photoreceptor Innermentioning

confidence: 59%

“…A key question in photoreceptor signaling is related to understanding the mechanisms that compress the 4-5 log unit dynamic range of phototransduction in the OS to the approximately 25-fold range for exocytosis in the photoreceptor terminal (Choi et al, 2005). Presynaptic [Ca 2+ ]i represents the final common path for this signal compression.…”

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confidence: 99%

The dynamic range and domain-specific signals of intracellular calcium in photoreceptors

Szikra

Križaj²

2006

Neuroscience

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“…6b) because they were rarer overall and correlated with higher contrasts rather than occurring randomly (Figs. [3][4][5]. The relation between the specific information (i, bits) and Q e , the number of vesicles comprising the event, could be described as a power function with an exponent of ~3, indicating that larger synaptic events transmitted more information per vesicle.…”

Section: The Amplitude Code Improves the Temporal Resolution Of Synapmentioning

confidence: 99%

“…those driven by spikes by the presence of a specialized structure, the ribbon, that holds tens of vesicles just behind the active zone 8,9 . It has been generally assumed that ribbon synapses represent the strength of the incoming stimulus in the form of a rate code generated by changes in the frequency of release events composed of one quantum of neurotransmitter contained within a vesicle 5,[10][11][12] . But it is also known that when these synapses are activated strongly several vesicles can be released within a few milliseconds [13][14][15] .…”

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confidence: 99%

An amplitude code transmits information at a visual synapse

et al. 2019

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Most neurons transmit information digitally using spikes that trigger release of synaptic vesicles with low probability. The first stages of vision and hearing are distinct in operating with analogue signals, but it is unclear how these are recoded for synaptic transmission. By imaging the release of glutamate in live zebrafish, we demonstrate that ribbon synapses of retinal bipolar cells encode contrast through changes in both the frequency and amplitude of release events. Higher contrasts caused multiple vesicles to be released within an event, and such coding by amplitude often continued after the rate code had reached a maximum frequency. Glutamate packets equivalent to five vesicles transmitted four times as many bits of information per vesicle compared to those released individually. By discretizing analogue signals into sequences of numbers up to about eleven, ribbon synapses can increase the dynamic range, temporal precision and efficiency with which visual information is transmitted. The spike code of neurons has been studied in detail 1,2 but much less is known about the vesicle code transmitting information across the synapse 3. Since the work of Katz 4 , the general view has been that changes in presynaptic potential are communicated by modulating the mean rate of a Poisson Process in which vesicles at the active zone are triggered to fuse independently 5,6. At most synapses, the voltage signal controlling this process is digital, arriving in the form of an all-or-none spike, and the output is also digital, in the form of a vesicle releasing a fixed packet of neurotransmitter. But in the first stages of vision and hearing the neural signal is in analogue form-continuous changes in membrane potential that are graded with the strength of the stimulus 7. How are these sensory signals recoded for transmission across a synapse?

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“…Photoreceptor cells have the amazing ability to respond and adapt to a wide range of light intensities (1). To transmit this dynamic visual information, their presynaptic terminals form specialized structures called synaptic ribbons, which are present in retinal rod and cone photoreceptor cells, bipolar cells and inner ear sensory hair cells (2).…”

Section: Introductionmentioning

confidence: 99%

Zebrafish Cacna1fa is required for cone photoreceptor function and synaptic ribbon formation

Jia

Muto

Orisme

et al. 2014

Human Molecular Genetics

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Mutations in the human CACNA1F gene cause incomplete congenital stationary night blindness type 2 (CSNB2), a non-progressive, clinically heterogeneous retinal disorder. However, the molecular mechanisms underlying CSNB2 have not been fully explored. Here, we describe the positional cloning of a blind zebrafish mutant, wait until dark (wud), which encodes a zebrafish homolog of human CACNA1F. We identified two zebrafish cacna1f paralogs and showed that the cacna1fa transcript (the gene mutated in wud) is expressed exclusively in the photoreceptor layer. We demonstrated that Cacna1fa localizes at the photoreceptor synapse and is absent from wud mutants. Electroretinograms revealed abnormal cone photoreceptor responses from wud mutants, indicating a defect in synaptic transmission. Although there are no obvious morphological differences, we found that wud mutants lacked synaptic ribbons and that wud is essential for the development of synaptic ribbons. We found that Ribeye, the most prominent synaptic ribbon protein, was less abundant and mislocalized in adult wud mutants. In addition to cloning wud, we identified synaptojanin 1 (synj1) as the defective gene in slacker (slak), a blind mutant with floating synaptic ribbons. We determined that Cacna1fa was expressed in slak photoreceptors and that Synj1 was initially expressed wud photoreceptors, but was absent by 5 days postfertilization. Collectively, our data demonstrate that Cacna1fa is essential for cone photoreceptor function and synaptic ribbon formation and reveal a previously unknown yet critical role of L-type voltage-dependent calcium channels in the expression and/or distribution of synaptic ribbon proteins, providing a new model to study the clinical variability in human CSNB2 patients.

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Encoding Light Intensity by the Cone Photoreceptor Synapse

Cited by 14 publications

References 0 publications

The dynamic range and domain-specific signals of intracellular calcium in photoreceptors

The dynamic range and domain-specific signals of intracellular calcium in photoreceptors

An amplitude code transmits information at a visual synapse

Zebrafish Cacna1fa is required for cone photoreceptor function and synaptic ribbon formation

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