scholarly journals A novel Ca2+-feedback mechanism extends the operating range of mammalian rods to brighter light

2015 ◽  
Vol 146 (4) ◽  
pp. 307-321 ◽  
Author(s):  
Frans Vinberg ◽  
Teemu T. Turunen ◽  
Hanna Heikkinen ◽  
Marja Pitkänen ◽  
Ari Koskelainen
Keyword(s):  
Light Adaptation ◽  
Visual Stimuli ◽  
High Gain ◽  
Feedback Mechanism ◽  
Sensory Cells ◽  
Ambient Light ◽  
Rod Photoreceptors ◽  
Background Stimulation ◽  
Flash Response ◽  
Dependent Mechanism

Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual photons, but remain responsive to visual stimuli under conditions of bright ambient light, which would be expected to saturate their response given the high gain of the rod transduction cascade in darkness. These photoreceptors regulate their sensitivity to light rapidly and reversibly in response to changes in ambient illumination, thereby avoiding saturation. Calcium ions (Ca2+) play a major role in mediating the rapid, subsecond adaptation to light, and the Ca2+-binding proteins GCAP1 and GCAP2 (or guanylyl cyclase–activating proteins [GCAPs]) have been identified as important mediators of the photoreceptor response to changes in intracellular Ca2+. However, mouse rods lacking both GCAP1 and GCAP2 (GCAP−/−) still show substantial light adaptation. Here, we determined the Ca2+ dependency of this residual light adaptation and, by combining pharmacological, genetic, and electrophysiological tools, showed that an unknown Ca2+-dependent mechanism contributes to light adaptation in GCAP−/− mouse rods. We found that mimicking the light-induced decrease in intracellular [Ca2+] accelerated recovery of the response to visual stimuli and caused a fourfold decrease of sensitivity in GCAP−/− rods. About half of this Ca2+-dependent regulation of sensitivity could be attributed to the recoverin-mediated pathway, whereas half of it was caused by the unknown mechanism. Furthermore, our data demonstrate that the feedback mechanisms regulating the sensitivity of mammalian rods on the second and subsecond time scales are all Ca2+ dependent and that, unlike salamander rods, Ca2+-independent background-induced acceleration of flash response kinetics is rather weak in mouse rods.

scholarly journals Calcium regulates some, but not all, aspects of light adaptation in rod photoreceptors.

1989 ◽  
Vol 94 (2) ◽  
pp. 233-259 ◽  
Author(s):  
G D Nicol ◽  
M D Bownds
Keyword(s):  
Light Adaptation ◽  
Calcium Ionophore ◽  
Absolute Magnitude ◽  
Calcium Ionophore A23187 ◽  
Background Intensity ◽  
Ionophore A23187 ◽  
Background Illumination ◽  
Rod Photoreceptors ◽  
Time To Peak ◽  
Flash Response

The role of calcium as a regulator of light adaptation in rod photoreceptors was examined by manipulation of the intracellular Ca2+ concentration through the use of the calcium ionophore A23187 and external Ca2+ buffers. These studies utilized suspensions of isolated and purified frog rod outer segments that retain their mitochondria-rich inner segments (OS-IS). Three criteria of the dark- and light-adapted flash response were characterized as a function of the Ca2+ concentration: (a) the time to peak, (b) the rate of recovery, and (c) the response amplitude or sensitivity. For all Ca2+ concentrations examined, the time to peak of the flash response was accelerated in the presence of background illumination, suggesting that mechanisms controlling this aspect of adaptation are independent of the Ca2+ concentration. The recovery kinetics of the flash response appeared to depend on the Ca2+ concentration. In 1 mM Ca2+-Ringer's and 300 nM Ca2+-Ringer's + A23187, background illumination enhanced the recovery rate of the response; however, in 10 and 100 nM Ca2+-Ringer's + A23187, the recovery rates were the same for dark- and light-adapted responses. This result implies that a critical level of Ca2+ may be necessary for background illumination to accelerate the recovery of the flash response. The sensitivity of the flash response in darkness (SDF) was dependent on the Ca2+ concentration. In 1 mM Ca2+-Ringer's SDF was 0.481 pA per bleached rhodopsin (Rh*); a background of four Rh*/s decreased SDF by half (Io). At 300 nM Ca2+ + A23187, SDF was reduced to 0.0307 pA/Rh* and Io increased to 60 Rh*/s. At 100 nM Ca2+ + A23187, SDF was reduced further to 0.0025 pA/Rh* and Io increased to 220 Rh*/s. In 10 nM Ca2+ + A23187, SDF was lowered to 0.00045 pA/Rh* and Io raised to 760 RhI/s. Using these values of SDF and Io for each respective Ca2+ concentration, the dependence of the flash sensitivity on background intensity could be described by the Weber-Fechner relation. Under low Ca2+ conditions + A23187, bright background illumination could desensitize the flash response. These results are consistent with the idea that the concentration of Ca2+ may set the absolute magnitude of response sensitivity in darkness, and that there exist mechanisms capable of adapting the photoresponse in the absence of significant changes in cytoplasmic Ca2+ concentration.

scholarly journals Variation in Rhodopsin Kinase Expression Alters the Dim Flash Response Shut Off and the Light Adaptation in Rod Photoreceptors

2011 ◽  
Vol 52 (9) ◽  
pp. 6793 ◽  
Author(s):  
Keisuke Sakurai ◽  
Joyce E. Young ◽  
Vladimir J. Kefalov ◽  
Shahrokh C. Khani
Keyword(s):  
Light Adaptation ◽  
Rod Photoreceptors ◽  
Rhodopsin Kinase ◽  
Kinase Expression ◽  
Flash Response

scholarly journals Light adaptation in retinal rods of the rabbit and two other nonprimate mammals.

1991 ◽  
Vol 97 (3) ◽  
pp. 413-435 ◽  
Author(s):  
K Nakatani ◽  
T Tamura ◽  
K W Yau
Keyword(s):  
Light Adaptation ◽  
Evoked Responses ◽  
Flash Intensity ◽  
Exponential Form ◽  
Time To Peak ◽  
Outward Currents ◽  
Retinal Rods ◽  
Response Peak ◽  
Flash Response ◽  
Plateau Level

The responses of rabbit rods to light were studied by drawing a single rod outer segment projecting from a small piece of retina into a glass pipette to record membrane current. The bath solution around the cells was maintained at near 40 degrees C. Light flashes evoked transient outward currents that saturated at up to approximately 20 pA. One absorbed photon produced a response of approximately 0.8 pA at peak. At the rising phase of the flash response, the relation between response amplitude and flash intensity (IF) had the exponential form 1-e-kappa FIF (where kappa F is a constant denoting sensitivity) expected from the absence of light adaptation. At the response peak, however, the amplitude-intensity relation fell slightly below the exponential form. At times after the response peak, the deviation was progressively more substantial. Light steps evoked responses that rose to a transient peak and rapidly relaxed to a lower plateau level. The response-intensity relation again indicated that light adaptation was insignificant at the early rising phase of the response, but became progressively more prominent at the transient peak and the steady plateau of the response. Incremental flashes superposed on a steady light of increasing intensity evoked responses that had a progressively shorter time-to-peak and faster relaxation, another sign of light adaptation. The flash sensitivity changed according to the Weber-Fechner relation (i.e., inversely) with background light intensity. We conclude that rabbit rods adapt to light in a manner similar to rods in cold-blooded vertebrates. Similar observations were made on cattle and rat rods.

scholarly journals Novel Form of Adaptation in Mouse Retinal Rods Speeds Recovery of Phototransduction

2003 ◽  
Vol 122 (6) ◽  
pp. 703-712 ◽  
Author(s):  
Claudia M. Krispel ◽  
Ching-Kang Chen ◽  
Melvin I. Simon ◽  
Marie E. Burns
Keyword(s):  
Dark Current ◽  
Bright Light ◽  
Ambient Light ◽  
Rate Limiting Step ◽  
Limiting Step ◽  
Electrophysiological Recordings ◽  
Bright Flash ◽  
Retinal Rods ◽  
Rate Limiting ◽  
Flash Response

Photoreceptors of the retina adapt to ambient light in a manner that allows them to detect changes in illumination over an enormous range of intensities. We have discovered a novel form of adaptation in mouse rods that persists long after the light has been extinguished and the rod's circulating dark current has returned. Electrophysiological recordings from individual rods showed that the time that a bright flash response remained in saturation was significantly shorter if the rod had been previously exposed to bright light. This persistent adaptation did not decrease the rate of rise of the response and therefore cannot be attributed to a decrease in the gain of transduction. Instead, this adaptation was accompanied by a marked speeding of the recovery of the response, suggesting that the step that rate-limits recovery had been accelerated. Experiments on knockout rods in which the identity of the rate-limiting step is known suggest that this adaptive acceleration results from a speeding of G protein/effector deactivation.

scholarly journals Regulation of cGMP levels by guanylate cyclase in truncated frog rod outer segments.

1989 ◽  
Vol 94 (4) ◽  
pp. 649-668 ◽  
Author(s):  
S Kawamura ◽  
M Murakami
Keyword(s):  
Guanylate Cyclase ◽  
Outer Segment ◽  
Time Course ◽  
Light Adaptation ◽  
Light Response ◽  
Regulation Mechanism ◽  
Maximal Effect ◽  
Rod Outer Segment ◽  
Light Flashes ◽  
Dependent Mechanism

Cyclic GMP is the second messenger in phototransduction and regulates the photoreceptor current. In the present work, we tried to understand the regulation mechanism of cytoplasmic cGMP levels in frog photoreceptors by measuring the photoreceptor current using a truncated rod outer segment (tROS) preparation. Since exogenously applied substance diffuses into tROS from the truncated end, we could examine the biochemical reactions relating to the cGMP metabolism by manipulating the cytoplasmic chemical condition. In tROS, exogenously applied GTP produced a dark current whose amplitude was half-maximal at approximately 0.4 mM GTP. The conductance for this current was suppressed by light in a fashion similar to when it is activated by cGMP. In addition, no current was produced in the absence of Mg2+, which is known to be necessary for the guanylate cyclase activity. These results indicate that guanylate cyclase was present in tROS and synthesized cGMP from exogenously applied GTP. The enzyme activity was distributed throughout the rod outer segment. The amount of synthesized cGMP increased as the cytoplasmic Ca2+ concentration of tROS decreased, which indicated the activation of guanylate cyclase at low Ca2+ concentrations. Half-maximal effect of Ca2+ was observed at approximately 100 nM. tROS contained the proteins involved in the phototransduction mechanism and therefore, we could examine the regulation of the light response waveform by Ca2+. At low Ca2+ concentrations, the time course of the light response was speeded up probably because cGMP recovery was facilitated by activation of the cyclase. Then, if the cytoplasmic Ca2+ concentration of a photoreceptor decreases during light stimulation, the Ca2+ decrease may explain the acceleration of the light response during light adaptation. In tROS, however, we did observe an acceleration during repetitive light flashes when the cytoplasmic Ca2+ concentration increased during the stimulation. This result suggests the presence of an additional light-dependent mechanism that is responsible for the acceleration of the light response during light adaptation.

scholarly journals Onset of Feedback Reactions Underlying Vertebrate Rod Photoreceptor Light Adaptation

1998 ◽  
Vol 111 (1) ◽  
pp. 39-51 ◽  
Author(s):  
Peter D. Calvert ◽  
Theresa W. Ho ◽  
Yvette M. LeFebvre ◽  
Vadim Y. Arshavsky
Keyword(s):  
Guanylate Cyclase ◽  
Light Adaptation ◽  
Continuous Illumination ◽  
Enzymatic Reactions ◽  
Rod Photoreceptor ◽  
Cgmp Phosphodiesterase ◽  
Rhodopsin Kinase ◽  
Slow Dissociation ◽  
Kinetics Of ◽  
Flash Response

Light adaptation in vertebrate photoreceptors is thought to be mediated through a number of biochemical feedback reactions that reduce the sensitivity of the photoreceptor and accelerate the kinetics of the photoresponse. Ca2+ plays a major role in this process by regulating several components of the phototransduction cascade. Guanylate cyclase and rhodopsin kinase are suggested to be the major sites regulated by Ca2+. Recently, it was proposed that cGMP may be another messenger of light adaptation since it is able to regulate the rate of transducin GTPase and thus the lifetime of activated cGMP phosphodiesterase. Here we report measurements of the rates at which the changes in Ca2+ and cGMP are followed by the changes in the rates of corresponding enzymatic reactions in frog rod outer segments. Our data indicate that there is a temporal hierarchy among reactions that underlie light adaptation. Guanylate cyclase activity and rhodopsin phosphorylation respond to changes in Ca2+ very rapidly, on a subsecond time scale. This enables them to accelerate the falling phase of the flash response and to modulate flash sensitivity during continuous illumination. To the contrary, the acceleration of transducin GTPase, even after significant reduction in cGMP, occurs over several tens of seconds. It is substantially delayed by the slow dissociation of cGMP from the noncatalytic sites for cGMP binding located on cGMP phosphodiesterase. Therefore, cGMP-dependent regulation of transducin GTPase is likely to occur only during prolonged bright illumination.

scholarly journals Locomotion induces stimulus-specific response enhancement in adult visual cortex

2017 ◽  
Author(s):  
Megumi Kaneko ◽  
Yu Fu ◽  
Michael P. Stryker
Keyword(s):  
Visual Cortex ◽  
Visual Stimuli ◽  
High Gain ◽  
Specific Response ◽  
Single Neurons ◽  
Visual Responses ◽  
Intrinsic Signal ◽  
Non Invasive ◽  
Response Enhancement ◽  
Visual Cortical

SUMMARYThe responses of neurons in the visual cortex (V1) of adult mammals have long been thought to be stable over long periods. Here, we investigated whether repeated exposure to specific stimuli would enhance V1 visual responses in mice using intrinsic signal imaging through the intact skull and two-photon imaging of calcium signals in single neurons. Mice ran on Styrofoam balls floating on air while viewing one of three different, high-contrast visual stimuli. V1 responses to the stimuli that were viewed by the animal were specifically enhanced, while responses to other stimuli were unaffected. Similar exposure in stationary mice, or in mice in which NMDA receptors were partially blocked, did not significantly enhance responses. These findings indicate that stimulus-specific plasticity in the adult visual cortex depends on concurrent locomotion, presumably as a result of the high-gain state of visual cortex induced by locomotion.Significance StatementWe report a rapid and persistent increase in visual cortical responses to visual stimuli presented during locomotion in intact mice. We first used a method that is completely non-invasive, intrinsic signal imaging through the intact skull. We then measured the same effects on single neurons using 2-photon calcium imaging and found that the increase in response to a particular stimulus produced by locomotion depends on how well the neuron is initially driven by the stimulus. To our knowledge, this is the first time such enhancement has been described in single neurons or using non-invasive measurements.

scholarly journals Light adaptation and dark adaptation of human rod photoreceptors measured from thea-wave of the electroretinogram

1999 ◽  
Vol 518 (2) ◽  
pp. 479-496 ◽  
Author(s):  
M. M. Thomas ◽  
T. D. Lamb
Keyword(s):  
Dark Adaptation ◽  
Light Adaptation ◽  
Rod Photoreceptors

scholarly journals Exchange of Cone for Rod Phosphodiesterase 6 Catalytic Subunits in Rod Photoreceptors Mimics in Part Features of Light Adaptation

2015 ◽  
Vol 35 (24) ◽  
pp. 9225-9235 ◽  
Author(s):  
A. Majumder ◽  
J. Pahlberg ◽  
H. Muradov ◽  
K. K. Boyd ◽  
A. P. Sampath ◽  
...  
Keyword(s):  
Light Adaptation ◽  
Rod Photoreceptors ◽  
Catalytic Subunits
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