Transmission of single photon signals through a binary synapse in the mammalian retina

2004 ◽  
Vol 21 (5) ◽  
pp. 693-702 ◽  
Author(s):  
AMY BERNTSON ◽  
ROBERT G. SMITH ◽  
W. ROWLAND TAYLOR
Keyword(s):  
Ganglion Cells ◽  
Single Photon ◽  
Bipolar Cells ◽  
Single Photons ◽  
Rod Photoreceptors ◽  
Neural Noise ◽  
Light Levels ◽  
Retinal Circuitry ◽  
Binary Event ◽  
Rod Bipolar Cells

At very low light levels the sensitivity of the visual system is determined by the efficiency with which single photons are captured, and the resulting signal transmitted from the rod photoreceptors through the retinal circuitry to the ganglion cells and on to the brain. Although the tiny electrical signals due to single photons have been observed in rod photoreceptors, little is known about how these signals are preserved during subsequent transmission to the optic nerve. We find that the synaptic currents elicited by single photons in mouse rod bipolar cells have a peak amplitude of 5–6 pA, and that about 20 rod photoreceptors converge upon each rod bipolar cell. The data indicates that the first synapse, between rod photoreceptors and rod bipolar cells, signals a binary event: the detection, or not, of a photon or photons in the connected rod photoreceptors. We present a simple model that demonstrates how a threshold nonlinearity during synaptic transfer allows transmission of the single photon signal, while rejecting the convergent neural noise from the 20 other rod photoreceptors feeding into this first synapse.

Optimization of Single-Photon Response Transmission at the Rod-to-Rod Bipolar Synapse

Physiology ◽  
2007 ◽  
Vol 22 (4) ◽  
pp. 279-286 ◽  
Author(s):  
Haruhisa Okawa ◽  
Alapakkam P. Sampath
Keyword(s):  
Light Absorption ◽  
Single Photon ◽  
Absolute Threshold ◽  
Bipolar Cells ◽  
Physiological Mechanisms ◽  
Rod Photoreceptors ◽  
Dim Light ◽  
Single Photon Response ◽  
Rod Bipolar Cells

Our ability to see in dim light is limited by the statistics of light absorption in rod photoreceptors and the faithful transmission of the light-evoked signals through the retina. This article reviews the physiological mechanisms at the synapse between rods and rod bipolar cells, the first relay in a pathway that mediates vision near absolute threshold.

scholarly journals Evolution of vertebrate retinal photoreception

2009 ◽  
Vol 364 (1531) ◽  
pp. 2911-2924 ◽  
Author(s):  
Trevor D. Lamb
Keyword(s):  
Ganglion Cells ◽  
Deep Ocean ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Low Light ◽  
Vertebrate Retina ◽  
Light Levels ◽  
Retinal Circuitry ◽  
Shed Light

Recent findings shed light on the steps underlying the evolution of vertebrate photoreceptors and retina. Vertebrate ciliary photoreceptors are not as wholly distinct from invertebrate rhabdomeric photoreceptors as is sometimes thought. Recent information on the phylogenies of ciliary and rhabdomeric opsins has helped in constructing the likely routes followed during evolution. Clues to the factors that led the early vertebrate retina to become invaginated can be obtained by combining recent knowledge about the origin of the pathway for dark re-isomerization of retinoids with knowledge of the inability of ciliary opsins to undergo photoreversal, along with consideration of the constraints imposed under the very low light levels in the deep ocean. Investigation of the origin of cell classes in the vertebrate retina provides support for the notion that cones, rods and bipolar cells all originated from a primordial ciliary photoreceptor, whereas ganglion cells, amacrine cells and horizontal cells all originated from rhabdomeric photoreceptors. Knowledge of the molecular differences between cones and rods, together with knowledge of the scotopic signalling pathway, provides an understanding of the evolution of rods and of the rods' retinal circuitry. Accordingly, it has been possible to propose a plausible scenario for the sequence of evolutionary steps that led to the emergence of vertebrate photoreceptors and retina.

scholarly journals The Optimal Synapse for Sparse, Binary Signals in the Rod Pathway

2006 ◽  
Vol 18 (1) ◽  
pp. 26-44 ◽  
Author(s):  
Paul T. Clark ◽  
Mark C. W. van Rossum
Keyword(s):  
Transfer Function ◽  
Signal To Noise Ratio ◽  
Bipolar Cells ◽  
Signal To Noise ◽  
Low Light ◽  
Rod Photoreceptors ◽  
Light Levels ◽  
Noise Ratio ◽  
Simulated Images ◽  
Rod Bipolar Cells

The sparsity of photons at very low light levels necessitates a nonlinear synaptic transfer function between the rod photoreceptors and the rod-bipolar cells. We examine different ways to characterize the performance of the pathway: the error rate, two variants of the mutual information, and the signal-to-noise ratio. Simulation of the pathway shows that these approaches yield substantially different performance at very low light levels and that maximizing the signal-to-noise ratio yields the best performance when judged from simulated images. The results are compared to recent data.

scholarly journals Activation of rod input in a model of retinal degeneration reverses retinal remodeling and induces formation of normal synapses, circuitry and visual signaling in the adult retina

2018 ◽  
Author(s):  
Tian Wang ◽  
Johan Pahlberg ◽  
Jon Cafaro ◽  
Alapakkam P. Sampath ◽  
Greg D. Field ◽  
...  
Keyword(s):  
Synaptic Transmission ◽  
Retinal Ganglion Cells ◽  
Bipolar Cell ◽  
Ganglion Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Retinal Ganglion ◽  
Rod Photoreceptors ◽  
Retinal Remodeling ◽  
Rod Bipolar Cells

AbstractA major cause of human blindness is the death of rod photoreceptors. As rods degenerate, synaptic structures between rod and rod bipolar cells dissolve and the rod bipolar cells extend their dendrites and occasionally make aberrant contacts. Such changes are broadly observed in blinding disorders caused by photoreceptor cell death and is thought to occur in response to deafferentation. How the remodeled retinal circuit affect visual processing following rod rescue is not known. To address this question, we generated transgenic mice wherein a disrupted cGMP-gated channel (CNG) gene can be repaired at the endogenous locus and at different stages of degeneration by tamoxifen-inducible cre-mediated recombination. In normal rods, light-induced closure of CNG channels leads to hyperpolarization of the cell, reducing neurotransmitter release at the synapse. Similarly, rods lacking CNG channel exhibit a resting membrane potential that was ~10mV hyperpolarized compared to WT rods, indicating diminished glutamate release. Retinas from these mice undergo stereotypic retinal remodeling as a consequence of rod malfunction and degeneration. Upon tamoxifen-induced expression of CNG channels, rods recovered their structure and exhibited normal light responses. Moreover, we show that the adult mouse retina displays a surprising degree of plasticity upon activation of rod input. Wayward bipolar cell dendrites establish contact with rods to support normal synaptic transmission, which is propagated to the retinal ganglion cells. These findings demonstrate remarkable plasticity extending beyond the developmental period and support efforts to repair or replace defective rods in patients blinded by rod degeneration.Significance StatementCurrent strategies for treatment of neurodegenerative disorders are focused on the repair of the primary affected cell type. However, the defective neuron functions within a complex neural circuitry, which also becomes degraded during disease. It is not known whether a rescued neuron and the remodeled circuit will establish communication to regain normal function. We show that the adult mammalian neural retina exhibits a surprising degree of plasticity following rescue of rod photoreceptors. The wayward rod bipolar cell dendrites re-establish contact with rods to support normal synaptic transmission, which is propagated to the retinal ganglion cells. These findings support efforts to repair or replace defective rods in patients blinded by rod cell loss.

scholarly journals The discovery of the ability of rod photoreceptors to signal single photons

2018 ◽  
Vol 150 (3) ◽  
pp. 383-388 ◽  
Author(s):  
Edward N. Pugh
Keyword(s):  
Visual System ◽  
Molecular Mechanism ◽  
Single Photon ◽  
Visual Environment ◽  
Single Photons ◽  
Rod Photoreceptors ◽  
Subsequent Research ◽  
Visual Threshold ◽  
Reliable Transmission

Vertebrate rod photoreceptors evolved the astonishing ability to respond reliably to single photons. In parallel, the proximate neurons of the visual system evolved the ability to reliably encode information from a few single-photon responses (SPRs) as arising from the presence of an object of interest in the visual environment. These amazing capabilities were first inferred from measurements of human visual threshold by Hecht et al. (1942), whose paper has since been cited over 1,000 times. Subsequent research, in part inspired by Hecht et al.’s discovery, has directly measured rod SPRs, characterized the molecular mechanism responsible for their generation, and uncovered much about the specializations in the retina that enable the reliable transmission of SPRs in the teeth of intrinsic neuronal noise.

Unique functional properties of the APB sensitive and insensitive rod pathways signaling light decrements in mouse retinal ganglion cells

2006 ◽  
Vol 23 (1) ◽  
pp. 127-135 ◽  
Author(s):  
GUO-YONG WANG
Keyword(s):  
Functional Properties ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Clear Cut ◽  
Types Of Information ◽  
Rod Bipolar Cells ◽  
Rod Pathway ◽  
Cone Bipolar Cells

Light decrements are mediated by two distinct groups of rod pathways in the dark-adapted retina that can be differentiated on the basis of their sensitivity to the glutamate agonist DL-2-amino-phosphonobutyric (APB). By means of the APB sensitive pathway, rods transmit light decrementsviarod bipolar cells to AII amacrine cells, then to Off cone bipolar cells, which in turn innervate the dendrites of Off ganglion cells. APB hyperpolarizes rod bipolar cells, thus blocking this rod pathway. With APB insensitive pathways, rods either directly synapse onto Off cone bipolar cells, or rods pass light decrement signal to cones by gap junctions. In the present study, whole-cell patch-clamp recordings were made from ganglion cells in the dark-adapted mouse retina to investigate the functional properties of APB sensitive and insensitive rod pathways. The results revealed several clear-cut differences between the APB sensitive and APB insensitive rod pathways. The latency of Off responses to a flashing spot of light was significantly shorter for the APB insensitive pathways than those for the APB sensitive pathway. Moreover, Off responses of the APB insensitive pathways were found to be capable of following substantially higher stimulus frequencies. Nitric oxide was found to selectively block Off responses in the APB sensitive rod pathway. Collectively, these results provide evidence that the APB sensitive and insensitive rod pathways can convey different types of information signaling light decrements in the dark-adapted retina.

scholarly journals Synaptic circuits for irradiance coding by intrinsically photosensitive retinal ganglion cells

2018 ◽  
Author(s):  
Shai Sabbah ◽  
Carin Papendorp ◽  
Elizabeth Koplas ◽  
Marjo Beltoja ◽  
Cameron Etebari ◽  
...  
Keyword(s):  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Bipolar Cells ◽  
Retinal Ganglion ◽  
Electron Microscopic ◽  
Synaptic Circuits ◽  
Ribbon Synapses ◽  
High Pass ◽  
Excitatory Drive ◽  
Rod Bipolar Cells

SummaryWe have explored the synaptic networks responsible for the unique capacity of intrinsically photosensitive retinal ganglion cells (ipRGCs) to encode overall light intensity. This luminance signal is crucial for circadian, pupillary and related reflexive responses light. By combined glutamate-sensor imaging and patch recording of postsynaptic RGCs, we show that the capacity for intensity-encoding is widespread among cone bipolar types, including OFF types.Nonetheless, the bipolar cells that drive ipRGCs appear to carry the strongest luminance signal. By serial electron microscopic reconstruction, we show that Type 6 ON cone bipolar cells are the dominant source of such input, with more modest input from Types 7, 8 and 9 and virtually none from Types 5i, 5o, 5t or rod bipolar cells. In conventional RGCs, the excitatory drive from bipolar cells is high-pass temporally filtered more than it is in ipRGCs. Amacrine-to-bipolar cell feedback seems to contribute surprisingly little to this filtering, implicating mostly postsynaptic mechanisms. Most ipRGCs sample from all bipolar terminals costratifying with their dendrites, but M1 cells avoid all OFF bipolar input and accept only ectopic ribbon synapses from ON cone bipolar axonal shafts. These are remarkable monad synapses, equipped with as many as a dozen ribbons and only one postsynaptic process.

Distribution of protein kinase C isoforms in the cat retina

2002 ◽  
Vol 19 (5) ◽  
pp. 549-562 ◽  
Author(s):  
BOZENA FYK-KOLODZIEJ ◽  
WENHUI CAI ◽  
ROBERTA G. POURCHO
Keyword(s):  
Protein Kinase C ◽  
Protein Kinase ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Kinase C ◽  
Cat Retina ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells

Immunocytochemical localization was carried out for five isoforms of protein kinase C (PKC) in the cat retina. In common with other mammalian species, PKCα was found in rod bipolar cells. Staining was also seen in a small population of cone bipolar cells with axon terminals ramifying near the middle of the inner plexiform layer (IPL). PKCβI was localized to rod bipolar cells, one class of cone bipolar cell, and numerous amacrine and displaced amacrine cells. Staining for PKCβII was seen in three types of cone bipolar cells as well as in amacrine and ganglion cells. Immunoreactivity for both PKCε and PKCζ was found in rod bipolar cells; PKCε was also seen in a population of cone bipolar cells and a few amacrine and ganglion cells whereas PKCζ was found in all ganglion cells. Double-label immunofluorescence studies showed that dendrites of the two PKCβII-positive OFF-cone bipolar cells exhibit immmunoreactivity for the kainate-selective glutamate receptor GluR5. The third PKCβII cone bipolar is an ON-type cell and did not stain for GluR5. The retinal distribution of these isoforms of PKC is consistent with a role in modulation of various aspects of neurotransmission including synaptic vesicle release and regulation of receptor molecules.

scholarly journals Behavioural and physiological limits to vision in mammals

2017 ◽  
Vol 372 (1717) ◽  
pp. 20160072 ◽  
Author(s):  
Greg D. Field ◽  
Alapakkam P. Sampath
Keyword(s):  
Single Photon ◽  
Signal Transmission ◽  
High Sensitivity ◽  
Human Vision ◽  
Past Century ◽  
Single Photons ◽  
Rod Photoreceptors ◽  
Physiological Limits ◽  
Visual Threshold ◽  
Behavioural Experiments

Human vision is exquisitely sensitive—a dark-adapted observer is capable of reliably detecting the absorption of a few quanta of light. Such sensitivity requires that the sensory receptors of the retina, rod photoreceptors, generate a reliable signal when single photons are absorbed. In addition, the retina must be able to extract this information and relay it to higher visual centres under conditions where very few rods signal single-photon responses while the majority generate only noise. Critical to signal transmission are mechanistic optimizations within rods and their dedicated retinal circuits that enhance the discriminability of single-photon responses by mitigating photoreceptor and synaptic noise. We describe behavioural experiments over the past century that have led to the appreciation of high sensitivity near absolute visual threshold. We further consider mechanisms within rod photoreceptors and dedicated rod circuits that act to extract single-photon responses from cellular noise. We highlight how these studies have shaped our understanding of brain function and point out several unresolved questions in the processing of light near the visual threshold. This article is part of the themed issue ‘Vision in dim light’.

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