Neural and Photochemical Mechanisms of Visual Adaptation in the Rat

The effects of light adaptation on the increment threshold, rhodopsin content, and dark adaptation have been studied in the rat eye over a wide range of intensities. The electroretinogram threshold was used as a measure of eye sensitivity. With adapting intensities greater than 1.5 log units above the absolute ERG threshold, the increment threshold rises linearly with increasing adapting intensity. With 5 minutes of light adaptation, the rhodopsin content of the eye is not measurably reduced until the adapting intensity is greater than 5 log units above the ERG threshold. Dark adaptation is rapid (i.e., completed in 5 to 10 minutes) until the eye is adapted to lights strong enough to bleach a measurable fraction of the rhodopsin. After brighter light adaptations, dark adaptation consists of two parts, an initial rapid phase followed by a slow component. The extent of slow adaptation depends on the fraction of rhodopsin bleached. If all the rhodopsin in the eye is bleached, the slow fall of threshold extends over 5 log units and takes 2 to 3 hours to complete. The fall of ERG threshold during the slow phase of adaptation occurs in parallel with the regeneration of rhodopsin. The slow component of dark adaptation is related to the bleaching and resynthesis of rhodopsin; the fast component of adaptation is considered to be neural adaptation.     

THE INFLUENCE OF LIGHT ADAPTATION ON SUBSEQUENT DARK ADAPTATION OF THE EYE

The course of dark adaptation of the human eye varies with the intensity used for the light adaptation which precedes it. Preadaptation to intensities below 200 photons is followed only by rod adaptation, while preadaptation to intensities above 4000 photons is followed first by cone adaptation and then by rod adaptation. With increasing intensities of preadaptation, cone dark adaptation remains essentially the same in form, but covers an increasing range of threshold intensities. At the highest preadaptation the range of the subsequent cone dark adaptation covers more than 3 log units. Rod dark adaptation appears in two types—a rapid and a delayed. The rapid rod dark adaptation is evident after preadaptations to low intensities corresponding to those usually associated with rod function. The delayed rod dark adaptation shows up only after preadaptation to intensities which are hundreds of times higher than those which produce the maximal function of the rods in flicker, intensity discrimination, and visual acuity. The delayed form remains essentially constant in shape following different intensities of preadaptation. However, its time of appearance increases with the preadaptation intensity; after the highest preadaptation, it appears only after 12 or 13 minutes in the dark. These two modes of rod dark adaptation are probably the expression of two methods of formation of visual purple in the rods after its bleaching by the preadaptation lights.     

INTERMITTENT STIMULATION BY LIGHT : III. THE RELATION BETWEEN INTENSITY AND CRITICAL FUSION FREQUENCY FOR DIFFERENT RETINAL LOCATIONS

When measurements of the critical fusion frequency for white light over a large range of intensities are made with the rod-free area of the fovea, the relation between critical frequency and log I is given by a single sigmoid curve, the middle portion of which approximates a straight line whose slope is 11.0. This single relation must be a function of the foveal cones. When the measurements are made with a retinal area placed 5° from the fovea, and therefore containing both rods and cones, the relation between critical frequency and log I shows two clearly separated sections. At the lower intensities the relation is sigmoid and reaches an upper level at about 10 cycles per second, which is maintained for 1.25 log units, and is followed by another sigmoid relationship at the higher intensities similar to the one given by the rod-free area alone. These two parts of the data are obviously separate functions of the rods at low intensities and of the cones at high intensities. This is further borne out by similar measurements made with retinal areas 15° and 20° from the fovea where the ratio of rods to cones is anatomically greater than at 5°. The two sections of the data come out farther apart on the intensity scale, the rod portion being at lower intensities and the cone portion at higher intensities than at 5°. The general form of the relation between critical frequency and intensity is therefore determined by the relative predominance of the cones and the rods in the retinal area used for the measurements.     

Visual Adaptation in the Retina of the Skate

The electroretinogram (ERG) and single-unit ganglion cell activity were recorded from the eyecup of the skate (Raja erinacea and R. oscellata), and the adaptation properties of both types of response compared with in situ rhodopsin measurements obtained by fundus reflectometry. Under all conditions tested, the b-wave of the ERG and the ganglion cell discharge showed identical adaptation properties. For example, after flash adaptation that bleached 80% of the rhodopsin, neither ganglion cell nor b-wave activity could be elicited for 10–15 min. Following this unresponsive period, thresholds fell rapidly; by 20 min after the flash, sensitivity was within 3 log units of the dark-adapted level. Further recovery of threshold was slow, requiring an additional 70–90 min to reach absolute threshold. Measurements of rhodopsin levels showed a close correlation with the slow recovery of threshold that occurred between 20 and 120 min of dark adaptation; there is a linear relation between rhodopsin concentration and log threshold. Other experiments dealt with the initial unresponsive period induced by light adaptation. The duration of this unresponsive period depended on the brightness of the adapting field; with bright backgrounds, suppression of retinal activity lasted 20–25 min, but sensitivity subsequently returned and thresholds fell to a steady-state value. At all background levels tested, increment thresholds were linearly related to background luminance.     

The Electroretinogram of a Diurnal Gecko

Using the electroretinogram as the criterion of retinal activity the flicker fusion frequency, course of dark adaptation, and spectral sensitivity of the pure cone retina of the diurnal gecko, Phelsuma inunguis, were investigated. Both the curve relating flicker fusion frequency to stimulus intensity and that relating the amplitude of the flicker response to stimulus intensity showed a break as the intensity was increased. The dark adaptation curve was that typical of cone retinae; there was no break, adaptation was relatively rapid, and there was a total increase of sensitivity of only about 3 log units. The spectral sensitivity curve showed two maxima, a major one at about 560 mµ and another at about 460 mµ. Chromatic adaptation with red and blue lights demonstrated the presence of two independent mechanisms. Although red adaptation could not have had a direct effect on the pigment responsible for the "blue" mechanism the sensitivity of this mechanism was depressed by red adaptation. The possible relationships of the two mechanisms are discussed.     

DARK ADAPTATION IN DINEUTES

The level of dark adaptation of the whirligig beetle can be measured in terms of the threshold intensity calling forth a response. The course of dark adaptation was determined at levels of light adaptation of 6.5, 91.6, and 6100 foot-candles. All data can be fitted by the same curve. This indicates that dark adaptation follows parts of the same course irrespective of the level of light adaptation. The intensity of the adapting light determines the level at which dark adaptation will begin. The relation between log aI ₀ (instantaneous threshold) and log of adapting light intensity is linear over the range studied.     

The Duplex Nature of the Retina of the Nocturnal Gecko as Reflected in the Electroretinogram

The effect of light and dark adaptation on the electrical activity in two species of nocturnal gecko, Hemidactylus turcicus and Tarentola mauritanica was studied. The electroretinogram of both species changes from the scotopic type in the dark-adapted state to the photopic type after strong light adaptation. For the scotopic response fusion frequencies up to 18 flashes per sec. are obtained in both species. For the photopic response fusion frequencies up to 50 flashes per sec. are seen in Tarentola, and up to 25 flashes per sec. in Hemidactylus. Proceeding from dark to light adaptation the increment threshold (dI) is measured at different levels of adaptive illumination (I). At low levels of illumination the dI/I ratio is found to be small and at high levels of illumination to be large. No difference in the dI/I ratio is obtained for test lights of 462 and 605 mµ. During dark adaptation the change of threshold after exposure to moderate and weak lights (up to 10³ times dark threshold) is rather fast. After light adaptation to strong light (10⁶ times dark threshold) duplex dark adaptation curves are seen with a break separating a fast and a slow phase of dark adaptation. The significance of these results from a retina which possesses sense cells of only one type is discussed.     

THE DARK ADAPTATION OF RETINAL FIELDS OF DIFFERENT SIZE AND LOCATION

The decrease in threshold shown by the eye during dark adaptation proceeds in two steps. The first is rapid, short in duration, and small in extent. The second is slow, prolonged, and large. The first is probably due to cone function; the second to rod function. In centrally located fields the two parts of adaptation change differently with area. With small, foveal fields the first part dominates and only traces of the second part appear. As the area increases the first part changes a little, while the second part covers an increasing range of intensities and appears sooner in time. Measurements with an annulus field covering only the circumference of a 20° circle show most of the characteristics of a 20° whole field centrally located. Similarly a 2° field located at different distances from the center shows dark adaptation characteristics essentially like those of large centrally located fields whose edges correspond to the position of the central field. Evidently the behavior in dark adaptation of centrally located fields of different size is determined in the main not by area as area, but by the fact that the retina gradually changes in sensitivity from center to periphery, and therefore the larger the field the farther it reaches into peripheral regions of permanently greater sensibility.     

Functional classification of neurons of the cat inferior colliculus on the basis of temporal characteristics

We investigated the impulse activity of 103 neurons in cats anesthetized with a mixture of chloralose and urethane. The following response characteristics were studied in detail: 1) the latent period of the first impulse as a function of tone intensity; 2) threshold as a function of duration; 3) the frequency-threshold curves under the action of short (1–2 msec) and long (100–200 msec) tones; 4) the discharge "pattern" and the number of impulses under the action of signals with different durations and intensities. We demonstrated that the temporal characteristics of different neurons exhibit substantial differences. The high positive correlation among the temporal characteristics investigated enabled us to distinguish three groups of neurons. The first group was characterized by the following properties: a) short latent periods with a threshold tone intensity; 2) a short summation time (or none at all); 3) similarity of the frequency-threshold curves for short and long signals; 4) an initial on-discharge of 1–3 impulses. The second group was characterized by: 1) long latent periods with a threshold tone intensity; 2) pronounced temporal summation; 3) steeper frequency-threshold curves when the tone duration was increased; 4) prolonged discharge.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 2, pp. 137–146, September–October, 1969.     

Properties of visual cells in the lateral eye of Limulus in situ.

Excitatory properties of visual cells in the lateral eye of Limulus, investigated by optic nerve recordings in situ, differ significantly from the properties of cells in the classical, excised eye preparation. The differences suggest the possibility that two receptor mechanisms function in the eye in situ: one mechanism encodes low light intensities and the other responds to high intensities. The two mechanisms enable each ommatidium to respond over an intensity range of approximately 10 log units. This hypothesis was tested by measuring the increment threshold and the spectral sensitivity, by studying light and dark adaptation, and by analyzing the variability of the impulse discharge. Although the results do not conclusively identify two receptor mechanisms, they indicate that a process or a part of a process that functions in the eye in situ is abolished by excising the eye or cutting off its blood supply.     

Effect of winter cold duration on spring phenology of the orange tip butterfly,Anthocharis cardamines

The effect of spring temperature on spring phenology is well understood in a wide range of taxa. However, studies on how winter conditions may affect spring phenology are underrepresented. Previous work on Anthocharis cardamines (orange tip butterfly) has shown population‐specific reaction norms of spring development in relation to spring temperature and a speeding up of post‐winter development with longer winter durations. In this experiment, we examined the effects of a greater and ecologically relevant range of winter durations on post‐winter pupal development of A. cardamines of two populations from the United Kingdom and two from Sweden. By analyzing pupal weight loss and metabolic rate, we were able to separate the overall post‐winter pupal development into diapause duration and post‐diapause development. We found differences in the duration of cold needed to break diapause among populations, with the southern UK population requiring a shorter duration than the other populations. We also found that the overall post‐winter pupal development time, following removal from winter cold, was negatively related to cold duration, through a combined effect of cold duration on diapause duration and on post‐diapause development time. Longer cold durations also lead to higher population synchrony in hatching. For current winter durations in the field, the A. cardamines population of southern UK could have a reduced development rate and lower synchrony in emergence because of short winters. With future climate change, this might become an issue also for other populations. Differences in winter conditions in the field among these four populations are large enough to have driven local adaptation of characteristics controlling spring phenology in response to winter duration. The observed phenology of these populations depends on a combination of winter and spring temperatures; thus, both must be taken into account for accurate predictions of phenology.     

The effect of sound intensity on duration-tuning characteristics of bat inferior collicular neurons

Previous studies have shown that inferior collicular neurons of the big brown bat, Eptesicus fuscus, serve as short-, band-, long- and all-pass filters for sound durations. Neurons with band-, short- and long-pass filtering characteristics discharged maximally to a specific sound duration or a range of sound durations. In contrast, neurons with all-pass filtering characteristics do not have duration selectivity. To determine if duration-tuning characteristics of collicular neurons were tolerant to changes in sound intensity, we examined the duration-tuning characteristics of collicular neurons using a wide range of sound intensities. Duration-tuning characteristics examined included the type, bandwidth and slope of duration-tuning curves. Sound intensity delivered within 20 dB of minimum threshold did not affect duration-tuning characteristics of all collicular neurons studied. Sound intensities at still higher levels did not affect the tuning characteristics of two-thirds of collicular neurons but decreased the duration selectivity and changed the duration-tuning curves of the remaining one-third of neurons from one type to another. However, these two groups of duration-tuning collicular neurons were not separately organized inside the inferior colliculus. The biological relevance of these findings to bat echolocation is discussed.     

Ecological Consequences of Long-Term Exposure of Anabaena variabilis (Cyanophyceae) to Shifts in Environmental Factors

Cultures of Anabaena variabilis were exposed to different light intensities, and the time course of photoadaptation was measured by photosynthetic rate and changes in pigmentation. A shift down in intensity of 284 μEin · m⁻² · sec⁻¹ caused a temporary decrease in the photosynthetic response followed by gradual adaptation to the new conditions. Final chlorophyll a and carotenoid concentrations were reached after 1 day, although other physiological indicators showed that adaptation required 4 days. The parameter I_k was shown to be the best indicator of photoadaptation. A shift up in light intensity of the same magnitude also required 4 days for complete photoadaptation by the culture, although chlorophyll and carotenoid concentrations stabilized within 1 day. A shift down in light intensity of 392 μEin · m⁻² · sec⁻¹ resulted in a temporary attempt to adapt followed by collapse of the population. This demonstrates an apparent threshold in the magnitude of the shift in light intensity which will permit successful adaptation. Simultaneous changes in light intensity and temperature also adversely affected culture populations. Our observations present a possible cause for the decline or prevention of an algal bloom under a fluctuating light regime and suggest that it may be possible to predict this decline as a result of synoptic weather patterns or hydrodynamic influences.     

On the role of horizontal cells in the mechanism of retinal adaptation

We recorded by intracellular means responses of horizontal cells of the turtle retina to light increase and decrease of different values against the starting adapting level. In measuring these responses, curves reflecting the dependence of membrane potential deflection on light intensity (amplitude characteristics — ACh) were plotted. It is demonstrated that the ACh of transitional processes (on- and off-peaks) is considerably steeper than ACh of the plateau of the potential, but embraces a much smaller range of light intensities (slightly more than 1 log. un.). During a change in intensity of the adapting background (up to 3 log. un.), the ACh of transitional processes shifts along the scale of light intensities in such a way that its steep part remains in the zone of adapting light. We followed the dynamics in time of ACh shift after the transition from one adapting brightness to another. The ACh of total impulse response was plotted for ganglionic cells of the turtle at different intensities of adapting light. Comparison of these curves with the ACh of horizontal cells shows that its peripheral components are responsible for adaptive shifts of ACh of the visual system and that horizontal cells play an important role in the mechanism of adaptation. It is hypothesized that adaptive ACh shifts are the consequence of positive feedback between the horizontal cells and receptors.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 1, No. 2, pp. 210–218, September–October, 1969.     

The effect of light adaptation on the dynamic properties of phototransduction in the fly,Phormia regina

The static and dynamic characteristics of phototransduction were studied in photoreceptors of the compound eye of the fly Phormia regina (Calliphoridae) using a green light emitting diode driven by a controlled current source. The LED provides sufficiently intense light to investigate the behaviour of the receptors over about half of the dark adapted range of the response versus log intensity curve. The effects of constant adapting light intensities upon the step response and upon the frequency response and coherence functions were examined. Using both methods the effect of light adaptation upon receptor sensitivity can be closely approximated by a similar linear dependence of log sensitivity upon log adapting intensity. However, there was no reliably detectable effect of light adaptation upon the time constant of the response over the range of adapting intensities used.Abbreviation LED Light Emitting Diode     

Frequency of seeing functions for intensity discrimination of various levels of adapting intensity

1. The percentage of times a human subject detects an increment (ΔI) in intensity was determined as a function of the magnitude of the increment and the magnitude of the stimulus (I) to which the increment is added. 2. Foveal stimulation was used, and five frequency of seeing curves were obtained at each of nine values of adapting intensity covering the range from –1.45 to 4.45 log photons. Each frequency of seeing curve shows the percentage of times an increment in intensity is detected as a function of the logarithm of the increment. 3. The slope of the frequency of seeing curve increases slightly with an increase in I and finally becomes independent of I at medium to high intensities. 4. The implications of the results for quantum theories of visual excitation are considered.     

Quantitative Studies on Pigment Migration and Light Sensitivity in the Compound Eye at Different Light Intensities

Comparative electrophysiological and histological studies were made on the functional significance of the secondary iris pigment migration for the sensitivity of the eye in the noctuid moth Cerapteryx graminis. The pigment position at different adapting light intensities was studied as well as the influence of different positions on the sensitivity of the eye. Adapting light intensities above a certain value hold the pigment in light position. At a 3 log units lower intensity the pigment is brought into dark position and at light intensities between these limiting values the pigment attains intermediate positions. The results indicate that at light intensities between the limiting values the pigment shifts closely follow the changes in intensity of the environmental light. With the pigment in dark position the eye is about 1000 times more sensitive than when the pigment is in light position, there being a close relationship between the sensitivity of the eye and the position of the pigment at intermediate positions.     

Single and Multiple Visual Systems in Arthropods

Extraction of two visual pigments from crayfish eyes prompted an electrophysiological examination of the role of visual pigments in the compound eyes of six arthropods. The intact animals were used; in crayfishes isolated eyestalks also. Thresholds were measured in terms of the absolute or relative numbers of photons per flash at various wavelengths needed to evoke a constant amplitude of electroretinogram, usually 50 µv. Two species of crayfish, as well as the green crab, possess blue- and red-sensitive receptors apparently arranged for color discrimination. In the northern crayfish, Orconectes virilis, the spectral sensitivity of the dark-adapted eye is maximal at about 550 mµ, and on adaptation to bright red or blue lights breaks into two functions with λ_max respectively at about 435 and 565 mµ, apparently emanating from different receptors. The swamp crayfish, Procambarus clarkii, displays a maximum sensitivity when dark-adapted at about 570 mµ, that breaks on color adaptation into blue- and red-sensitive functions with λ_max about 450 and 575 mµ, again involving different receptors. Similarly the green crab, Carcinides maenas, presents a dark-adapted sensitivity maximal at about 510 mµ that divides on color adaptation into sensitivity curves maximal near 425 and 565 mµ. Each of these organisms thus possesses an apparatus adequate for at least two-color vision, resembling that of human green-blinds (deuteranopes). The visual pigments of the red-sensitive systems have been extracted from the crayfish eyes. The horse-shoe crab, Limulus, and the lobster each possesses a single visual system, with λ_max respectively at 520 and 525 mµ. Each of these is invariant with color adaptation. In each case the visual pigment had already been identified in extracts. The spider crab, Libinia emarginata, presents another variation. It possesses two visual systems apparently differentiated, not for color discrimination but for use in dim and bright light, like vertebrate rods and cones. The spectral sensitivity of the dark-adapted eye is maximal at about 490 mµ and on light adaptation, whether to blue, red, or white light, is displaced toward shorter wavelengths in what is essentially a reverse Purkinje shift. In all these animals dark adaptation appears to involve two phases: a rapid, hyperbolic fall of log threshold associated probably with visual pigment regeneration, followed by a slow, almost linear fall of log threshold that may be associated with pigment migration.     

Correspondences in the Behavior of the Electroretinogram and of the Potentials Evoked at the Visual Cortex

Electrical potentials from the eye (ERG) and from the contralateral visual cortex were recorded in response to flashes of white and of colored light of various intensities and durations. The evoked potentials were found to parallel the behavior of the ERG in several significant respects. Selective changes in the ERG brought about by increasing the light intensity and by light adaptation led to parallel selective changes in the cortical responses. The dual waves (b₁, b₂) of the ERG were found to have counterparts in two cortical waves (c₁, c₂) which, in respect to changes in light intensity and to light adaptation, behaved analogously to the two retinal components. The responses evoked at high intensity showed only the diphasic c₁-potential. As stimulus intensity was lowered the c₁-wave decreased in magnitude and a delayed c₂-component appeared. The c₂-potential increased in amplitude as light intensity of the flash was further reduced. Eventually the c₂-wave, too, decreased as stimulus reduction continued. There was no wave length specificity in regard to either the duplex b-waves or duplex cortical waves. Both appeared at all wave lengths from 454 mµ to 630 mµ. The two cortical waves evoked by brief flashes of colored light showed all the behavior to changes in stimulus intensity and to light adaptation that occurred with white light.     

THE ORIENTATION OF ANIMALS BY OPPOSED BEAMS OF LIGHT

When orientation is attained under the influence of beams of parallel light opposed at 180° the deflection θ from a path at right angles to the beams is given by tan See PDF for Equation, where I ₁ and I ₂ are the photic intensities and H is the average angle between the photoreceptive surfaces. This expression is independent of the units in which I is measured, and holds whether the primary photosensory effect is proportional to I or to log I. When photokinetic side-to-side motions of the head occur, H decreases with increasing total acting light intensity, but increases if higher total light intensity restricts the amplitude of random movements; in each case, H is very nearly proportional to log I ₁ I ₂. For beams of light at 90°, See PDF for Equation. The application of these equations to some particular instances is discussed, and it is shown why certain simpler empirical formulæ previously found by others yield fair concordance with the experimental data. The result is thus in complete accord with the tropism theory, since the equations are based simply on the assumption that when orientation is attained photic excitation is the same on the two sides.