scholarly journals Properties of multi-vesicular release from rod photoreceptors support transmission of single photon responses

2021 ◽  
Author(s):  
CL Hays ◽  
AL Sladek ◽  
GD Field ◽  
WB Thoreson
Keyword(s):  
Poisson Process ◽  
Single Photon ◽  
Glutamate Release ◽  
Bipolar Cells ◽  
Resting Membrane Potential ◽  
Rod Photoreceptors ◽  
Voltage Change ◽  
Single Photon Response ◽  
Rebound Increase ◽  
Stimulus Offset

AbstractVision under starlight requires rod photoreceptors to transduce and transmit single photon responses to the visual system. This remarkable sensitivity depends on a small voltage change reliably reducing glutamate release such that post-synaptic rod bipolar cells can robustly detect the signal. To transmit this small signal, we have found that rod vesicle release deviates strongly from a Poisson process under conditions that mimic darkness. Specifically, at their resting membrane potential in darkness, rods exhibit coordinated and regularly timed multivesicular release events. Each release event consisted of ∼17 vesicles and occurred 2-3 times more regularly than expected from a Poisson process. Hyperpolarizing rods to mimic the voltage change produced by a single photon response abruptly reduced the probability of multivesicular release nearly to zero with a rebound increase in release probability at stimulus offset. Simulations of these release dynamics indicate that this regularly timed, multivesicular release promotes transmission of single photon responses to post-synaptic neurons. Furthermore, the mechanism is efficient, requiring fewer vesicles to be released per second than uniquantal release governed by Poisson statistics.

scholarly journals Properties of multi-vesicular release from mouse rod photoreceptors support transmission of single photon responses

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Cassandra L Hays ◽  
Asia L Sladek ◽  
Greg D Field ◽  
Wallace B Thoreson
Keyword(s):  
Single Photon ◽  
Glutamate Release ◽  
Bipolar Cells ◽  
Resting Membrane Potential ◽  
Rod Photoreceptors ◽  
Poisson Statistics ◽  
Voltage Change ◽  
Vesicular Release ◽  
Rebound Increase ◽  
Stimulus Offset

Vision under starlight requires rod photoreceptors transduce and transmit single photon responses to the visual system. Small single photon voltage changes must therefore cause detectable reductions in glutamate release. We found that rods achieve this by employing mechanisms that enhance release regularity and its sensitivity to small voltage changes. At the resting membrane potential in darkness, mouse rods exhibit coordinated and regularly timed multivesicular release events, each consisting of ~17 vesicles and occurring 2-3 times more regularly than predicted by Poisson statistics. Hyperpolarizing rods to mimic the voltage change produced by a single photon abruptly reduced the probability of multivesicular release nearly to zero with a rebound increase at stimulus offset. Simulations of these release dynamics indicate that this regularly timed, multivesicular release promotes transmission of single photon responses to post-synaptic rod bipolar cells. Furthermore, the mechanism is efficient, requiring lower overall release rates than uniquantal release governed by Poisson statistics.

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.

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.

scholarly journals Position of rhodopsin photoisomerization on the disk surface confers variability to the rising phase of the single photon response in vertebrate rod photoreceptors

PLoS ONE ◽  
2020 ◽  
Vol 15 (10) ◽  
pp. e0240527
Author(s):  
Giovanni Caruso ◽  
Colin J. Klaus ◽  
Heidi E. Hamm ◽  
Vsevolod V. Gurevich ◽  
Clint L. Makino ◽  
...  
Keyword(s):  
Single Photon ◽  
Disk Surface ◽  
Rod Photoreceptors ◽  
Single Photon Response

scholarly journals Nano-optical single-photon response mapping of waveguide integrated molybdenum silicide (MoSi) superconducting nanowires

2016 ◽  
Vol 24 (13) ◽  
pp. 13931 ◽  
Author(s):  
Jian Li ◽  
Robert A. Kirkwood ◽  
Luke J. Baker ◽  
David Bosworth ◽  
Kleanthis Erotokritou ◽  
...  
Keyword(s):  
Single Photon ◽  
Molybdenum Silicide ◽  
Superconducting Nanowires ◽  
Response Mapping ◽  
Single Photon Response

Altered desensitization produces enhancement of EPSPs in neocortical neurons

1994 ◽  
Vol 72 (2) ◽  
pp. 1032-1036 ◽  
Author(s):  
M. R. Pelletier ◽  
J. J. Hablitz
Keyword(s):  
Nmda Receptors ◽  
Time Course ◽  
Glutamate Release ◽  
Epileptiform Activity ◽  
Brain Slices ◽  
Synaptic Activity ◽  
Membrane Properties ◽  
Repetitive Firing ◽  
Resting Membrane Potential ◽  
Bath Application

1. Neocortical brain slices were prepared from rats (35–50 days of age) and maintained in vitro. Intracellular recordings were obtained from neurons in cortical layers II/III. The effect of bath application of cyclothiazide (CYZ), a potent blocker of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor desensitization, on evoked synaptic activity and passive membrane properties was investigated. 2. Bath application of CYZ did not significantly affect resting membrane potential, input resistance, or repetitive firing. CYZ increased both the amplitude and duration of evoked excitatory postsynaptic potentials (EPSPs). Polysynaptic responses were also augumented. These effects persisted after the blockade of N-methyl-D-aspartate (NMDA) receptors with D-2-amino-5-phosphonovaleric acid (D-APV). The magnitude of these effects appeared to vary directly with stimulation intensity and presumably, amount of glutamate release. 3. Epileptiform activity was induced by bath application of bicuculline methiodide. The amplitude and duration of evoked paroxysmal discharges were increased by CYZ. Similar results were seen in presence of D-APV. 4. These results indicate that CYZ has significant effects on synaptic transmission. Desensitization of non-NMDA receptors may be an important mechanism for determining the time course of EPSPs and in curtailing epileptiform responses in the rat neocortex.

Spontaneous Oscillatory Activity of Starburst Amacrine Cells in the Mouse Retina

2005 ◽  
Vol 94 (3) ◽  
pp. 1770-1780 ◽  
Author(s):  
Jerome Petit-Jacques ◽  
Béla Völgyi ◽  
Bernardo Rudy ◽  
Stewart Bloomfield
Keyword(s):  
Feedback Inhibition ◽  
Glutamate Release ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Kainate Receptors ◽  
Oscillatory Activity ◽  
Mouse Retina ◽  
Inner Plexiform Layer ◽  
Experimental Conditions ◽  
Starburst Amacrine Cells

Using patch-clamp techniques, we investigated the characteristics of the spontaneous oscillatory activity displayed by starburst amacrine cells in the mouse retina. At a holding potential of –70 mV, oscillations appeared as spontaneous, rhythmic inward currents with a frequency of ∼3.5 Hz and an average maximal amplitude of ∼120 pA. Application of TEA, a potassium channel blocker, increased the amplitude of oscillatory currents by >70% but reduced their frequency by ∼17%. The TEA effects did not appear to result from direct actions on starburst cells, but rather a modulation of their synaptic inputs. Oscillatory currents were inhibited by 6-cyano-7-nitroquinoxalene-2,3-dione (CNQX), an antagonist of AMPA/kainate receptors, indicating that they were dependent on a periodic glutamatergic input likely from presynaptic bipolar cells. The oscillations were also inhibited by the calcium channel blockers cadmium and nifedipine, suggesting that the glutamate release was calcium dependent. Application of AP4, an agonist of mGluR6 receptors on on-center bipolar cells, blocked the oscillatory currents in starburst cells. However, application of TEA overcame the AP4 blockade, suggesting that the periodic glutamate release from bipolar cells is intrinsic to the inner plexiform layer in that, under experimental conditions, it can occur independent of photoreceptor input. The GABA receptor antagonists picrotoxin and bicuculline enhanced the amplitude of oscillations in starburst cells prestimulated with TEA. Our results suggest that this enhancement was due to a reduction of a GABAergic feedback inhibition from amacrine cells to bipolar cells and the resultant increased glutamate release. Finally, we found that some ganglion cells and other types of amacrine cell also displayed rhythmic activity, suggesting that oscillatory behavior is expressed by a number of inner retinal neurons.

scholarly journals Diffusion of the Second Messengers in the Cytoplasm Acts as a Variability Suppressor of the Single Photon Response in Vertebrate Phototransduction

2008 ◽  
Vol 94 (9) ◽  
pp. 3363-3383 ◽  
Author(s):  
Paolo Bisegna ◽  
Giovanni Caruso ◽  
Daniele Andreucci ◽  
Lixin Shen ◽  
Vsevolod V. Gurevich ◽  
...  
Keyword(s):  
Single Photon ◽  
Second Messengers ◽  
Single Photon Response

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.

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