The Time Course of Light Adaptation in Vertebrate Retinal Rods

AbstractThe phosphorylation of photoexcited rhodopsin (Rho*) is thought to inactivate this receptor by inhibiting its interaction with the GTP-binding protein transducin (Gt). Here we report that the time course of phosphorylation-dephosphorylation after bright illumination of intact rod outer and inner segments (ROS-RIS) incubated in 33Pi can be altered if the ROS-RIS are first exposed to levels of dim illumination that cause light adaptation in these ROS-RIS. The dephosphorylation of >107 phosphorylated rhodopsin molecules/ROS following a bright flash can be blocked by prior dim continuous illumination (generating 103 Rho*/ROS/s) that cumulatively bleaches ≍ 105 rhodopsin molecules/ROS. The phenomenon has not been previously noted because these low levels of light are emitted as a result of Cerenkov radiation from the 32P isotope that is usually employed to monitor rhodopsin phosphorylation. The inhibition of rhodopsin dephosphorylation by dim conditioning illumination is observed in intact ROS-RIS but is lost when ROS-RIS are electropermeabilized or fragmented.

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The Effect of Changed Extracellular Calcium and Sodium Concentration on the Electroretinogram of the Crayfish Retina

Zeitschrift für Naturforschung C ◽

10.1515/znc-1980-3-423 ◽

1980 ◽

Vol 35 (3-4) ◽

pp. 308-318 ◽

Cited By ~ 12

Author(s):

H. Stieve ◽

I. Claßen-Linke

Keyword(s):

Dark Adaptation ◽

Time Course ◽

Calcium Concentration ◽

Light Adaptation ◽

Sodium Concentration ◽

Strong Increase ◽

Calcium Stores ◽

Half Time ◽

Astacus Leptodactylus ◽

External Calcium

Abstract The electroretinogram (ERG) of the isolated retina of the crayfish Astacus leptodactylus evoked by strong 10 ms light flashes at constant 5 min intervals was measured while the retina was continuously superfused with various salines which differed in Ca2+ -and Na+ -concentrations. The osmotic pressure of test- and reference-saline was adjusted to be identical by adding sucrose. Results: 1. Upon raising the calcium-concentration of the superfusate in the range of 20-150 mmol/l (constant Na+ -concentration: 208 mmol/l) the peak amplitude hmax and the half time of decay t2 of the ERG both decrease gradually up to about 50% in respect to the corresponding value in reference saline. 2. The recovery of the ERG due to dark adaptation following the “weakly light adapted state” is greatly diminished in high external [Ca2+]ex. 3. Lowering the external calcium-concentration (10 →1 mmol/l) causes a small increase in hmax and a strong increase of the half time of decay t2 (about 180%). Upon lowering the calcium concentration of the superfusate to about 1 nmol/l by 1 mmol/l of the calcium buffer EDTA, a slowly augmenting diminution of the ERG height hm SLX occurs. However, a strong retardation of the falling phase of the ERG characterized by an increase in t2 occurs quickly. Even after 90 min stay in the low calcium saline the retina is still not inexcitable; hmax is 5 - 10% of the reference value. The diminution of hmax occurs about six-fold faster when the buffer concentration is raised to 10 mmol/l EDTA. 4. Additional lowering of the Na+ -concentration (208 →20.8 mmol/l) in a superfusate with a calcium concentration raised to 150 mmol/l causes a strong reduction of the ERG amplitude hmax to about 10%. 5. In a superfusate containing 1 nmol/l calcium such lowering of the sodium concentration (208 → 20.8 mmol/l) causes a diminution of the ERG height to about 40% and the shape of the ERG to become polyphasic; at least two maxima with different time to peak values are observed. Interpretation: 1. The similarity of effects, namely raising external calcium concentration and light adaptation on the one hand and lowering external calcium and dark adaptation on the other hand may indicate that the external calcium is acting on the adaptation mechanism of the photoreceptor cells, presumably by influencing the intracellular [Ca2+]. 2. The great tolerance of the retina against Ca2+ -deficiency in the superfusate might be effected by calcium stores in the retina which need high Ca2+ -buffer concentrations in the superfusate to become exhausted. 3. In contrast to the Limulus ventral nerve photoreceptor there does not seem to be an antagonis tic effect of sodium and calcium in the crayfish retina on the control of the light channels. 4. The crayfish receptor potential seems to be composed of at least two different processes. Lowering calcium-and lowering external sodium-concentration both diminish the height and change the time course of the two components to a different degree. This could be caused by in fluencing the state of adaptation and thereby making the two maxima separately visible.

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Changes of Acuity during Light and Dark Adaptation in the Dragonfly Compound Eye

Zeitschrift für Naturforschung C ◽

10.1515/znc-1990-1-226 ◽

1990 ◽

Vol 45 (1-2) ◽

pp. 137-142 ◽

Cited By ~ 3

Author(s):

Eric J. Warrant ◽

Robert B. Pinter

Keyword(s):

Dark Adaptation ◽

Time Course ◽

Light Adaptation ◽

Compound Eye ◽

Sensitivity Function ◽

The State ◽

Intracellular Recordings ◽

Acceptance Angle ◽

Angular Sensitivity ◽

Rapid Reduction

Abstract Intracellular recordings of angular sensitivity from the photoreceptors of Aeschnid dragonflies (Hemianax papuensis and Aeschna brevistyla) are used to determine the magnitude and time course of acuity changes following alterations of the state of light or dark adaptation. Acuity is defined on the basis of the acceptance angle, Δρ (the half-width of the angular-sensitivity function). The maximally light-adapted value of Δρ is half the dark-adapted value, indicating greater acuity during light adaptation. Following a change from light to dark adaptation, Δρ increases slowly, requiring at least 3 min to reach its dark-adapted value. In contrast, the reverse change (dark to light) induces a rapid reduction of Δρ , and at maximal adapting luminances, this reduction takes place in less than 10 sec.

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

The Journal of General Physiology ◽

10.1085/jgp.97.3.413 ◽

1991 ◽

Vol 97 (3) ◽

pp. 413-435 ◽

Cited By ~ 132

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.

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Two Temporal Phases of Light Adaptation in Retinal Rods

The Journal of General Physiology ◽

10.1085/jgp.119.2.129 ◽

2002 ◽

Vol 119 (2) ◽

pp. 129-146 ◽

Cited By ~ 34

Author(s):

Peter D. Calvert ◽

Victor I. Govardovskii ◽

Vadim Y. Arshavsky ◽

Clint L. Makino

Keyword(s):

Binding Sites ◽

Time Course ◽

Light Adaptation ◽

Dynamic Range ◽

Continuous Illumination ◽

Slow Phase ◽

Fast Phase ◽

Slow Adaptation ◽

Adaptation Phase

Vertebrate rod photoreceptors adjust their sensitivity as they adapt during exposure to steady light. Light adaptation prevents the rod from saturating and significantly extends its dynamic range. We examined the time course of the onset of light adaptation in bullfrog rods and compared it with the projected onset of feedback reactions thought to underlie light adaptation on the molecular level. We found that adaptation developed in two distinct temporal phases: (1) a fast phase that operated within seconds after the onset of illumination, which is consistent with most previous reports of a 1–2-s time constant for the onset of adaptation; and (2) a slow phase that engaged over tens of seconds of continuous illumination. The fast phase desensitized the rods as much as 80-fold, and was observed at every light intensity tested. The slow phase was observed only at light intensities that suppressed more than half of the dark current. It provided an additional sensitivity loss of up to 40-fold before the rod saturated. Thus, rods achieved a total degree of adaptation of ∼3,000-fold. Although the fast adaptation is likely to originate from the well characterized Ca2+-dependent feedback mechanisms regulating the activities of several phototransduction cascade components, the molecular mechanism underlying slow adaptation is unclear. We tested the hypothesis that the slow adaptation phase is mediated by cGMP dissociation from noncatalytic binding sites on the cGMP phosphodiesterase, which has been shown to reduce the lifetime of activated phosphodiesterase in vitro. Although cGMP dissociated from the noncatalytic binding sites in intact rods with kinetics approximating that for the slow adaptation phase, this hypothesis was ruled out because the intensity of light required for cGMP dissociation far exceeded that required to evoke the slow phase. Other possible mechanisms are discussed.

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Visual sensitivity across the menstrual cycle

Visual Neuroscience ◽

10.1017/s0952523804214031 ◽

2004 ◽

Vol 21 (4) ◽

pp. 513-531 ◽

Cited By ~ 22

Author(s):

ALVIN EISNER ◽

SARA N. BURKE ◽

MAUREEN D. TOOMEY

Keyword(s):

Oral Contraceptive ◽

Menstrual Cycle ◽

Time Course ◽

Light Adaptation ◽

Contraceptive Use ◽

Visual Sensitivity ◽

Visual Adaptation ◽

Hormonal Change ◽

Menstrual Cycles ◽

Sensitivity Change

This study was designed to evaluate the hypothesis that hormonal change can affect lower level light-adaptation processes, which are likely to be retinally based. Foveal visual sensitivities were measured across several menstrual cycles of four women not using hormonally acting medication and across several menstrual cycles of three women using a triphasic oral contraceptive. One woman, diagnosed with premenstrual syndrome (PMS), was a subject for both groups. Sensitivities were measured for a series of test wavelengths for 580-nm backgrounds of 2.0 and 4.0 log td. Of the six individuals tested, one had clear evidence of visual-adaptation changes occurring in phase with the menstrual cycle. Prior to using the oral contraceptive, this individual (the PMS subject) experienced changes of short-wavelength-sensitive (SWS)-cone-mediated sensitivities of up to about 1.4 log unit on the 4.0 log td background. Her SWS-cone-mediated sensitivities tended to be highest near ovulation and lowest premenstrually. Threshold-versus-illuminance (TVI) curves confirmed that the rate of sensitivity decrease with increasing background illuminance (i.e. the TVI slope) was greater premenstrually. The degree of background-induced desensitization within her middle-wavelength-sensitive (MWS)/long-wavelength-sensitive (LWS) cone pathways also appeared to vary cyclically, but the magnitude of the variation was smaller and the time course appeared to be different. When this subject began oral contraceptive use, the patterns of sensitivity change were all altered. None of the other five subjects experienced changes of SWS-cone-mediated vision that were cyclic and significantly adaptation-state dependent. However, there was evidence for a limited degree of cyclic adaptation change within the MWS/LWS cone pathways of at least one additional subject. We conclude that hormonal change can—for some unknown proportion of women—be linked to alterations of retinal function. However, the alterations are not the same for all visual pathways, and there are pronounced individual differences. The data also demonstrate that individuals' visual adaptation capabilities can vary substantially over periods of weeks.

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Properties of light adaptation in retinal rods

Experimental Eye Research ◽

10.1016/0014-4835(92)90452-x ◽

1992 ◽

Vol 55 ◽

pp. 71

Author(s):

L. Cervetto ◽

S. Bisti ◽

A. Campagni ◽

S. Del Bianco ◽

G.C. Demontis ◽

...

Keyword(s):

Light Adaptation ◽

Retinal Rods

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Effect of intracellularly applied sodium ions on the dark voltage of isolated retinal rods

Visual Neuroscience ◽

10.1017/s0952523800004533 ◽

1990 ◽

Vol 4 (4) ◽

pp. 331-336 ◽

Cited By ~ 4

Author(s):

Karl-Friedrich Schmidt ◽

Gottfried N. Nöll ◽

Christian Baumann

Keyword(s):

Calcium Ions ◽

Time Course ◽

Sodium Ions ◽

Sodium Calcium ◽

Retinal Rods ◽

High Calcium ◽

Simple Medium ◽

Cytoplasmic Content ◽

Calcium Exchange ◽

Sodium Effect

AbstractIsolated retinal rods of the frog consisting of the outer segment and the ellipsoid were patch-clamped and recorded in the whole-cell mode. The recording pipettes were filled with solutions of different composition in order to alter the cytoplasmic content of sodium, phosphate, and calcium ions, and guanine nucleotides. When a simple medium with potassium as the principal cation was used, the dark voltage slowly approached more negative values. This tendency of spontaneous hyperpolarization was reduced significantly when cGMP or GTP were present in the pipette medium. Sodium ions, on the other hand, clearly increased the speed of hyperpolarization. In the presence of sodium (20 mM), the stabilizing effect of GTP did not occur and that of cGMP was clearly diminished. Phosphate (20 mM) neutralized the sodium effect. High calcium levels (100 μM) did not measurably influence the time course of hyperpolarization. We conclude that the normal cytoplasmic sodium level in rods does not exceed 10 mM and that higher internal sodium concentrations interfere with the sodium–calcium exchange mechanism.

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Ionotropic GABA Receptors and Distal Retinal ON and OFF Responses

Scientifica ◽

10.1155/2014/149187 ◽

2014 ◽

Vol 2014 ◽

pp. 1-23 ◽

Cited By ~ 5

Author(s):

E. Popova

Keyword(s):

Gaba Receptors ◽

Time Course ◽

Light Adaptation ◽

Current Knowledge ◽

Relative Sensitivity ◽

Bipolar Cells ◽

Visual Signals ◽

Gamma Aminobutyric Acid ◽

Large Populations

In the vertebrate retina, visual signals are segregated into parallel ON and OFF pathways, which provide information for light increments and decrements. The segregation is first evident at the level of the ON and OFF bipolar cells in distal retina. The activity of large populations of ON and OFF bipolar cells is reflected in the b- and d-waves of the diffuse electroretinogram (ERG). The role of gamma-aminobutyric acid (GABA), acting through ionotropic GABA receptors in shaping the ON and OFF responses in distal retina, is a matter of debate. This review summarized current knowledge about the types of the GABAergic neurons and ionotropic GABA receptors in the retina as well as the effects of GABA and specific GABAAand GABACreceptor antagonists on the activity of the ON and OFF bipolar cells in both nonmammalian and mammalian retina. Special emphasis is put on the effects on b- and d-waves of the ERG as a useful tool for assessment of the overall function of distal retinal ON and OFF channels. The role of GABAergic system in establishing the ON-OFF asymmetry concerning the time course and absolute and relative sensitivity of the ERG responses under different conditions of light adaptation in amphibian retina is also discussed.

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

The Journal of General Physiology ◽

10.1085/jgp.94.4.649 ◽

1989 ◽

Vol 94 (4) ◽

pp. 649-668 ◽

Cited By ~ 29

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.

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