Gap-Junctional Coupling and Absolute Sensitivity of Photoreceptors in Macaque Retina

Hornstein, Eric P.; Verweij, Jan; Li, Peter H.; Schnapf, Julie L.

doi:10.1523/jneurosci.3416-05.2005

Cited by 112 publications

(156 citation statements)

References 48 publications

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“…Consistent with this finding, Hornstein et al (2005) demonstrated tracer and signal coupling between rods in the macaque retina, where rod-rod gap junctions were found in regions containing rod somas and passing rod axons. Not necessarily contradictory to this finding, Raviola and Gilula (1973) found rare gap junctions between rod spherules in the macaque retina.…”

Section: Introductionmentioning

confidence: 58%

“…In the macaque retina, Hornstein et al (2005) reported rod-rod tracer couplings with Neurobiotin, as well as rod-rod electrical couplings; those gap junctions were located in regions containing rod somas and axons. We observed that gap junctions between rod spherules were rare in the OPL of the macaque retina, confirming the findings of Raviola and Gilula (1973).…”

Section: Discussionmentioning

confidence: 99%

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Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Tsukamoto

Omi

2014

Front. Neuroanat.

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This study compared the types of OFF bipolar cells found in the macaque retina with those found in the mouse retina and determined whether these OFF bipolar cells make direct contacts with both rods and cones by serial section transmission electron microscopy. We performed scatter plots and cluster analysis of the morphological variables of their axon terminals such as the stratification level, the arbor thickness, the arbor area, and the number of ribbons. Five OFF bipolar cell types, including the recently discovered DB3b type, were identified in the macaque retina. The macaque OFF bipolar cell types FMB, DB1, DB2, DB3a, and DB3b corresponded to the mouse OFF bipolar cell types 2, 1, 4, 3a, and 3b, respectively. In addition to contacting rod bipolar cells, ~7% of rods in the macaque retina made basal contacts exclusively with one cell type, DB3b, whereas 18% of rods in the mouse retina made basal contacts with one or two of types, 3a, 3b, and 4. Approximately 3% of mouse rods were divergently connected to two OFF bipolar cells of different types, but macaque rods were solely connected to one OFF bipolar cell. Rod-rod gap junctions were localized at rod cell bodies and axons in the outer nuclear layer in both macaque and mouse retinas. The direct rod-OFF bipolar connection system is slightly more developed in the mouse retina than in the macaque retina, possibly as a fine-tuned adaptation to nocturnal conditions. This one-step direct synaptic pathway from rods to OFF bipolar cells may enhance the response speed to OFF light stimuli compared with more indirect pathways via rod-cone gap junctions (a two-step pathway) and via rod bipolar and AII amacrine cells (a three-step pathway).

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Section: Introductionmentioning

confidence: 58%

Section: Discussionmentioning

confidence: 99%

Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Tsukamoto

Omi

2014

Front. Neuroanat.

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“…Mammalian retina also exhibits interphotoreceptor coupling, including weak rod-rod coupling [43]. Photoreceptor coupling is mediated by connexons containing Cx36 [44].…”

Section: Photoreceptor Couplingmentioning

confidence: 99%

“…Photoreceptor coupling is mediated by connexons containing Cx36 [44]. Coupling can improve the signal to noise ratio, extend the dynamic range of the rod synapse, and enhance boundary detection by cones [43,[45][46][47]. Coupling also influences the kinetics of post-synaptic responses by contributing to band pass filtering at rod synapses [48].…”

Section: Photoreceptor Couplingmentioning

confidence: 99%

“…In mammalian retina, spread of depolarizing current through gap junctions into neighboring cones produces a slow, second component in the cone-driven EPSC [50]. Rods also couple to cones, sometimes quite strongly, and the spread of depolarizing current from one photoreceptor cell type to another can also contribute to shaping post-synaptic responses [43,51]. Although gap junction coupling contributes to slow response components in the rod-driven EPSC, coupling is not entirely responsible for the slow kinetics of exocytosis from amphibian rods, as slow release kinetics are also found in single enzymatically isolated rods [16].…”

Section: Photoreceptor Couplingmentioning

confidence: 99%

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Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

Thoreson

2007

Mol Neurobiol

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The ribbon synapse is a specialized structure that allows photoreceptors to sustain the continuous release of vesicles for hours upon hours and years upon years but also respond rapidly to momentary changes in illumination. Light responses of cones are faster than those of rods and, mirroring this difference, synaptic transmission from cones is also faster than transmission from rods. This review evaluates the various factors that regulate synaptic kinetics and contribute to kinetic differences between rod and cone synapses. Presynaptically, the release of glutamate-laden synaptic vesicles is regulated by properties of the synaptic proteins involved in exocytosis, influx of calcium through calcium channels, calcium release from intracellular stores, diffusion of calcium to the release site, calcium buffering, and extrusion of calcium from the cytoplasm. The rate of vesicle replenishment also limits the ability of the synapse to follow changes in release. Post-synaptic factors include properties of glutamate receptors, dynamics of glutamate diffusion through the cleft, and glutamate uptake by glutamate transporters. Thus, multiple synaptic mechanisms help to shape the responses of second-order horizontal and bipolar cells. KeywordsPhotoreceptor; Synaptic transmission; Glutamate; Calcium; Vesicles; Retina Vision begins with the transduction of light into membrane potential changes as the result of an enzymatic cascade occurring in the outer segments of rod and cone photoreceptors [1,2]. Light-evoked membrane potential changes are modified by voltage-dependent currents in the inner segment [3] and transmitted to second order bipolar and horizontal cells by changes in release of the neurotransmitter, L-glutamate, from the synaptic terminals of both rods and cones. Because all of the visual information available to downstream retinal neurons must first pass through the photoreceptor synapse, synaptic transmission from photoreceptors has a considerable impact on visual perception. The focus of this review is on mechanisms that shape the kinetics of synaptic transmission at synapses of rods and cones. Additional information on other physiological and anatomical characteristics of photoreceptor ribbon synapses can be found in recent reviews [4][5][6]. Differences in Rod and Cone KineticsRod and cone photoreceptors are tonically depolarized in darkness with membrane potentials of −35 to −45 mV that allow continuous release of the neurotransmitter, L-glutamate. Light onset causes photoreceptors to hyperpolarize by as much as 30 mV, leading to a reduction in

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Visual threshold is set by linear and nonlinear mechanisms in the retina that mitigate noise

Pahlberg

Sampath

2011

BioEssays

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Summary In sensory biology, a major outstanding question is how sensory receptor cells minimize noise while maximizing signal to set the detection threshold. This optimization could be problematic because the origin of both the signals and the limiting noise in most sensory systems is believed to lie in stimulus transduction. Signal processing in receptor cells can improve the signal-to-noise ratio. However, neural circuits can further optimize detection threshold by pooling signals from sensory receptor cells and processing them using a combination of linear and nonlinear filtering mechanisms. In the visual system, the noise limiting light detection has been assumed to arise from stimulus transduction in rod photoreceptors. In this context the evolutionary optimization of the signal-to-noise ratio in the retina has proven critical in allowing visual sensitivity to approach the limits set by the quantal nature of light. Here we discuss how noise in the mammalian retina is mitigated to allow for highly sensitive night vision.

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Gap-Junctional Coupling and Absolute Sensitivity of Photoreceptors in Macaque Retina

Cited by 112 publications

References 48 publications

Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas

Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

Visual threshold is set by linear and nonlinear mechanisms in the retina that mitigate noise

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