Diurnal modulation of photoreceptor potassium conductance in the locust

Single electrode clamp techniques demonstrated diurnal changes in photoreceptor membrane conductance, recorded intracellularly in the intact, dark-adapted retina of the locust Schistocerca gregaria. In the day, locust photoreceptors exhibited the membrane properties of fast cells, as previously defined in rapidly moving diurnal Diptera. Depolarization activated a powerful potassium conductance with two kinetic components, one rapidly activating close to resting potential and the other activating more slowly when further depolarized, giving a pronounced delayed rectification. There was little inactivation. At night, locust photoreceptors resembled slow cells, as defined in weakly flying crepuscular and nocturnal Diptera. Depolarization rapidly activated an outward current which then inactivated over 100 ms to reduce rectification. The change from day to night state was mimicked by applying 10 mM serotonin extracellularly to the retina. We conclude that the potassium conductances of locust photoreceptor membranes are modulated according to a diurnal rhythm, possibly by serotonin. This neuromodulation is used to match photoreceptor membrane properties to photic habitat. Our findings suggest a definite and potentially widespread function for serotonin as a mediator of diurnal changes in the insect visual system.     

Studies on the Relation between the Pigment Migration and the Sensitivity Changes during Dark Adaptation in Diurnal and Nocturnal Lepidoptera

The functional significance of the pigment migration in the compound insect eye during dark adaptation has been studied in diurnal and nocturnal Lepidoptera. Measurements of the photomechanical changes were made on sections of eyes which had been dark-adapted for varying periods of time. In some experiments the sensitivity changes during dark adaptation were first determined before the eye was placed in the fixation solution. No change in the position of the retinal pigment occurred in Cerapteryx graminis until the eye had been dark-adapted for about 5 minutes. The start of the migration was accompanied by the appearance of a break in the dark adaptation curve. During longer periods of dark adaptation the outward movement of the pigment proceeded in parallel with the change in sensitivity, the migration as well as the adaptive process being completed within about 30 minutes. In the diurnal insects chosen for the present study (Erebia, Argynnis) the positional changes of the retinal pigment were insignificant in comparison with the movement of the distal pigment in Cerapteryx graminis. On the basis of these observations the tentative hypothesis is put forward that the second phase of adaptive change in nocturnal Lepidoptera is mediated by the migration of the retinal pigment while the first phase is assumed to be produced by the resynthesis of some photochemical substance. In diurnal insects which have no appreciable pigment migration the biochemical events alone appear to be responsible for the increase in sensitivity during dark adaptation.     

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

The common backswimmer, Notonecta glauca, uses vision by day and night for functions such as underwater prey animal capture and flight in search of new habitats. Although previous studies have identified some of the physiological mechanisms facilitating such flexibility in the animal''s vision, neither the biophysics of Notonecta photoreceptors nor possible cellular adaptations are known. Here, we studied Notonecta photoreceptors using patch-clamp and intracellular recording methods. Photoreceptor size (approximated by capacitance) was positively correlated with absolute sensitivity and acceptance angles. Information rate measurements indicated that large and more sensitive photoreceptors performed better than small ones. Our results suggest that backswimmers are adapted for vision in both dim and well-illuminated environments by having open-rhabdom eyes with large intrinsic variation in absolute sensitivity among photoreceptors, exceeding those found in purely diurnal or nocturnal species. Both electrophysiology and microscopic analysis of retinal structure suggest two retinal subsystems: the largest peripheral photoreceptors provide vision in dim light and the smaller peripheral and central photoreceptors function primarily in sunlight, with light-dependent pigment screening further contributing to adaptation in this system by dynamically recruiting photoreceptors with varying sensitivity into the operational pool.     

亚洲玉米螟蛾趋光行为及复眼结构节律性研究

用行为实验和光学显微镜观察比较了夜间暗适应处理和日间暗适应处理的亚洲玉米螟蛾Ostrinia furnacalis(Guenee)趋光反应及小眼的显微结构。(1)夜间暗适应处理组的趋光反应率明显高于日间暗适应处理组。5个照度行为实验中,前者最高反应率达80%,最低23%,总反应率近48%,而后者分别只有35%、10%和21%。(2)夜间暗适应与日间暗适应的复眼其屏蔽色素分布大体相同,但小网膜细胞核的分布区域有明显差异,表明亚洲玉米螟蛾小眼结构变化存在一定的节律性。这种结构节律变化可能是导致趋光反应昼夜差异的原因之一。     

Did neural pooling for night vision lead to the evolution of neural superposition eyes?

Observations of the infrared deep pseudopupil, optical determinations of the corneal nodal point, and histological methods were used to relate the visual fields of individual rhabdomeres to the array of ommatidial optical axes in four insects with open rhabdoms: the tenebrionid beetle Zophobas morio, the earwig Forficula auricularia, the crane fly Tipula pruinosa, and the backswimmer Notonecta glauca.The open rhabdoms of all four species have a central pair of rhabdomeres surrounded by six peripheral rhabdomeres. At night, a distal pigment aperture is fully open and the rhabdom receives light over an angle approximately six times the interommatidial angle. Different rhabdomeres within the same ommatidium do not share the same visual axis, and the visual fields of the peripheral rhabdomeres overlap the optical axes of several near-by ommatidia. During the day, the pigment aperture is considerably smaller, and all rhabdomeres share the same visual field of about two interommatidial angles, or less, depending on the degree of light adaptation. The pigment aperture serves two functions: (1) it allows the circadian rhythm to switch between the night and day sampling patterns, and (2) it works as a light driven pupil during the day.Theoretical considerations suggest that, in the night eye, the peripheral retinula cells are involved in neural pooling in the lamina, with asymmetric pooling fields matching the visual fields of the rhabdomeres. Such a system provides high sensitivity for nocturnal vision, and the open rhabdom has the potential of feeding information into parallel spatial channels with different tradeoffs between resolution and sensitivity. Modification of this operational principle to suit a strictly diurnal life, makes the contractile pigment aperture superfluous, and decreasing angular sensitivities together with decreasing pooling fields lead to a neural superposition eye.Abbreviations DPP deep pseudopupil - LMC large monopolar cell     

Adaptations for vision in dim light: impulse responses and bumps in nocturnal spider photoreceptor cells (<Emphasis Type="Italic">Cupiennius</Emphasis><Emphasis Type="Italic">salei</Emphasis> Keys)

The photoreceptor cells of the nocturnal spider Cupiennius salei were investigated by intracellular electrophysiology. (1) The responses of photoreceptor cells of posterior median (PM) and anterior median (AM) eyes to short (2 ms) light pulses showed long integration times in the dark-adapted and shorter integration times in the light-adapted state. (2) At very low light intensities, the photoreceptors responded to single photons with discrete potentials, called bumps, of high amplitude (2–20 mV). When measured in profoundly dark-adapted photoreceptor cells of the PM eyes these bumps showed an integration time of 128 ± 35 ms (n = 7) whereas in dark-adapted photoreceptor cells of AM eyes the integration time was 84 ± 13 ms (n = 8), indicating that the AM eyes are intrinsically faster than the PM eyes. (3) Long integration times, which improve visual reliability in dim light, and large responses to single photons in the dark-adapted state, contribute to a high visual sensitivity in Cupiennius at night. This conclusion is underlined by a calculation of sensitivity that accounts for both anatomical and physiological characteristics of the eye.     

夜蛾复眼转化速度与光暗适应的时间关系

夜行蛾类的复眼,随光、暗适应时间而逐步转化,这种转化是可逆的.以屏蔽色素分布范围的大小为指标来判断复眼的转化速度得以下结果:1.从亮眼到暗眼:亮眼进入暗适应后其屏蔽色素随暗适应时间的增加而逐步向远心端方向集中.屏蔽色素的移动是减速进行的.暗适应开始后的前3分钟,每分钟移动百分率为10.7,当暗到10—15分钟时每分钟移动百分率为4.6,再暗到60—150分钟时每分钟移动百分率为0.7.屏蔽色素移动的速度个体间差异较大,完成全过程大多数个体需150分钟,少数个体只需60分钟,另有个别个体经过270分钟暗适应仍尚未完成全过程.2.从暗眼到亮眼:暗眼受光后,其屏蔽色素随光适应时间的增加而向近心端方向扩散,色素移动速度随时间的增加而减缓.转化全过程约需60分钟.     

Structure and function of the larval eye of the sawfly, Perga

The visual properties of the stemmata of fourth and fifth instar sawfly larvae have been investigated by means of intracellular electrophysiological recordings, interference-, light-, scanning, and transmission electron microscopy, and ray tracing techniques. Each larva possesses one pair of lateral ocelli consisting of biconvex lens, a clear-zone of corneagenous cells devoid of pigment, and a retina made up of groups of 8 retinula cells with a central and fused rhabdom. Migration of pigment during the night is predominantly radial, i.e. directed towards the periphery of the retinula cell. Vertical pigment movement occurs after exposure to bright sunlight for several hours. A circadian rhythm controls the sensitivity of single units, which at night show an increased sensitivity by 2 to 3 log units. The difference between the mean values of acceptance angles for light-adapted units (11·46 ± 5·1° S.D.) and dark-adapted ones (13·83 ± 6·8°) is not statistically significant. The wide range of acceptance angles, with 4·5° being the narrowest and 31° the widest, is explained by the optics of the single lens: there is a small region of highest resolution where light is well focused to a spot, but towards the outer edge of the cup-shaped eye the focusing becomes less accurate. Sawfly larvae turn their heads towards an approaching object if it subtends at least 4° of arc. This limit does not change over a range of 3 log units. A polarization sensitivity of up to 10 : 1 was determined electrophysiologically. Electron microscope studies of the rhabdom show a system of highly oriented microvilli which is thought to be responsible for the polarization sensitivity. Two different waveforms, both occurring after resting potentials of 40 to 70 mV, were found in electrophysiological recordings: (a) hyperpolarizations and (b) depolarizations. Throughout the study only depolarizing units were taken into consideration. These showed characteristics of both the compound eye and the ocellus.     

Pigment migration and illumination of single photoreceptors in a moth

Summary The relation between intensity of illumination of single photoreceptors and position of the screening pigment was studied in the compound eye of the moth Deilephila elpenor. The amplitude of the response to test flashes of white light was measured in 7 dark adapted photoreceptor cells with the screening pigment in the extreme distal and in a proximal position. The experiments demonstrate that the response amplitude of individual photoreceptors varies with the pigment position. The associated variation in screening effect was 1.0 to 1.9 log units.The research reported in this study was supported by Swedish Medical Research Council, Sällskapet för Medicinsk Forskning and Stifteisen Gustaf och Tyra Svenssons Minne.     

Screening pigment,aperture and sensitivity in the dung beetle superposition eye

Summary Sensitivity to light was investigated in the refracting superposition eye of the dung beetle Onitis alexis using electrophysiological measurements and optical modelling. Intracellular recordings were made from single retinula cells over 24-h periods, with cells light and dark adapted, in order to measure the response/intensity (V-LogI) functions. The combined effects of a circadian rhythm and light adaptation allow the determination of the relative contributions of screening-pigment migration and transduction gain to changes in sensitivity in the eye. Between the extremes of dark adaptation at night and light adaptation during the day, the maximum sensitivity change possible is at least 4 log units, of which approximately 2 log units can be accounted for by changes in the transduction gain and at least 2 log units by screening-pigment migration. The role of the superposition aperture (the number of facets that contribute light to one rhabdom) in 3 species of dung beetle was investigated with an optical ray-tracing model of the eye. The facets of the superposition aperture do not contribute light equally to the target rhabdom; except in one species, the greatest contribution comes from facets located away from both the centre and periphery of the aperture. Light adaptation increases the optical density of the superposition aperture and decreases its size.     

Comparative Studies on Dark Adaptation in the Compound Eyes of Nocturnal and Diurnal Lepidoptera

A comparative analysis has been carried out of the time course and range of dark adaptation in the compound eyes of some common butterflies and noctuid moths (Lepidoptera). The change in sensitivity of the eye during dark adaptation was determined by measurements of the intensity of illumination necessary to elicit an electrical response of a given magnitude of the eye. It was found that the curve for dark adaptation in the diurnal species was smooth. The range of adaptive change varied in different species but usually did not cover more than 1 to 1.5 log units. In the nocturnal species the dark adaptation was found to proceed in two phases. The first phase was usually completed in less than 10 minutes and covered a range of 1 to 1.5 log units. The second phase was more prolonged and covered a range of 2 to 3 log units. In some of the experiments on nocturnal species the second phase failed to appear. Measurements of the size of the response at different intensities showed that the intensity/amplitude relationship was the same in the light-adapted eye as in the dark-adapted eye. In the nocturnal insects the response of the eye in the light-adapted condition was about 20 per cent of that in the dark-adapted eye, while in diurnal insects it was about 60 per cent.     

Daily changes of structure,function and rhodopsin content in the compound eye of the crabHemigrapsus sanguineus

The compound eye of the crab hemigrapsus sanguineus undergoes daily changes in morphology as determined by light and electron microscopy, both in the quantity of chromophore substances studied by HPLC and in visual sensitivity as shown by electrophysiological techniques. 1. At a temperature of 20 degrees C, the rhabdom occupation ratio (ROR) of an ommatidial retinula was 11.6% (maximum) at midnight, 8.0 times larger than the minimum value at midday (1.4%). 2. Observations by freeze-fracture revealed that the densities of intra-membranous particles (9-11 nm in diameter) of rhabdomeric membrane were ca. 2000/microns 2 and ca. 3000/microns 2 for night and daytime compound eyes, respectively. 3. Screening pigment granules migrated longitudinally and aggregated at night, but dispersed during the day. Reflecting pigment granules migrate transversally in the proximal half of the reticula layer i.e. cytoplasmic extensions containing reflecting pigment granules squeeze between neighbouring retinula cells causing optical isolation (Fig. 4). Thus the screening pigment granules within the retinula cells show longitudinal migration and radial movement so that the daytime rhabdoms are closely surrounded by the pigment granules. 4. At 20 degrees C, the total amount of chromophore of the visual pigment (11-cis and all-trans-retinal) was 1.4 times larger at night than during the day i.e. 46.6 pmol/eye at midnight and 33.2 pmol/eye at midday. Calculations of the total surface area of rhabdomeric membrane, total number of intra-membranous particles in rhabdomeric membrane and the total number of chromophore molecules in a compound eye, indicate that a considerable amount of chromophore-protein complex exists outside the rhabdom during the day. 5. The change in rhabdom size and quantity of chromophore were highly dependent on temperature. At 10 degrees C both rhabdom size and amount of chromophore stayed close to daytime levels throughout the 24 hours. 6. The intracellularly determined relative sensitivity of the dark adapted night eye to a point source of light was about twice as high as the dark-adapted day eye. Most of the increase in the sensitivity is attributed primarily to the effect of reflecting pigment migration around the basement membrane and, secondarily, to the changes in the amount and properties of the photoreceptive membrane. The results form the basis of a detailed discussion as to how an apposition eye can function possibly as a night-eye.     

Sensitivity and dynamics of the pupil mechanism in two tenebrionid beetles

Using infrared reflectometry of the deep pseudopupil, we have measured the absolute sensitivity, the dynamic range and the speed of the pupil mechanism in the acone apposition eye of two tenebrionid beetles: Zophobas morio F. and Tenebrio molitor L. The following conclusions are made from the results:

1. There is a substantial difference in sensitivity of the pupil mechanism between the two beetle species. The pupil is about 5.3 log units more sensitive in Zophobas than in Tenebrio.
2. There is also a difference in sensitivity between day and night. Surprisingly, the sensitivity is higher at day-time, and the difference is about 0.5 log units in both Zophobas and Tenebrio.
3. Light adaptation is completed faster during daytime than at night in both Zophobas and Tenebrio, whereas dark adaptation is completed about equally fast both day and night in both species. The speed of the pupil response, however, is dependent on the preceding adaptation history.
4. The pupil mechanism in both species is under the influence of a circadian rhythm, which determines the size of the pupil aperture in such a way that the pupil is maximally open when dark-adapted at night, but only partially open when dark-adapted at daytime.

The differences in sensitivity and dynamics of the pupil mechanism between day and night are mainly due to the circadian rhythm setting the control range of the pupil aperture in both Zophobas and Tenebrio. The pupil differences between the two beetles are discussed regarding behavioural differences between the two species.     

Photoreceptor spectral sensitivities of the Small White butterfly <Emphasis Type="Italic">Pieris rapae crucivora</Emphasis> interpreted with optical modeling

The compound eye of the Small White butterfly, Pieris rapae crucivora, has four classes of visual pigments, with peak absorption in the ultraviolet, violet, blue and green, but electrophysiological recordings yielded eight photoreceptors classes: an ultraviolet, violet, blue, double-peaked blue, green, blue-suppressed-green, pale-red and deep-red class. These photoreceptor classes were identified in three types of ommatidia, distinguishable by the different eye shine spectra and fluorescence; the latter only being present in the eyes of males. We present here two slightly different optical models that incorporate the various visual pigments, the light-filtering actions of the fluorescent, pale-red and deep-red screening pigment, located inside or adjacent to the rhabdom, and the reflectance spectrum of the tapetum that abuts the rhabdom proximally. The models serve to explain the photoreceptor spectral sensitivities as well as the eye shine.     

Wooing during Day or Night is not the Same: an Experimental Study in the Wolf Spider Schizocosa malitiosa

Diurnal and nocturnal activity patterns shown by different species will strongly determine the characteristics of signals as well as the sensory channels used during sexual interactions. Despite this, few studies have experimentally tested the effects of lighting and time of day on courtship characteristics in arthropods. Previous studies have shown that the wolf spider Schizocosa malitiosa can be active during the day or at night. We tested whether the period of the day affects the sexual behavior of S. malitiosa, by pairing males and females under diurnal or nocturnal conditions. We carried out mating trials in diurnal and nocturnal conditions in arenas containing female refuges. In diurnal conditions, male leg shaking behavior occurred at higher rates and consisted of greater leg raising angles relatively to nocturnal conditions. We did not find differences in mounts and mount latency between both experimental groups. In nocturnal conditions, female attacks and emergence from refuges were higher. Also, although mount occurrence did not differ between the two treatments, mounts inside the refuge were more frequent in diurnal conditions. Results suggest behavioral flexibility in male courtship and female receptivity responses relative to the time of the day.     

The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment

BACKGROUND: The mammalian eye shows marked adaptations to time of day. Some of these modifications are not acute responses to short-term light exposure but rely upon assessments of the photic environment made over several hours. In the past, all attempts at a mechanistic understanding have assumed that these adaptations originate with light detection by one or other of the classical photoreceptor cells (rods or cones). However, previous work has demonstrated that the mammalian eye contains non-rod, non-cone photoreceptors. This study aimed to determine whether such photoreceptors contribute to retinal adaptation. RESULTS: In the human retina, second-order processing of signals originating in cones takes significantly longer at night than during the day. Long-term light exposure at night is capable of reversing this effect. Here, we employed the cone ERG as a tool to examine the properties of the irradiance measurement pathway driving this reversal. Our findings indicate that this pathway (1) integrates irradiance measures over time periods ranging from at least 15 to 120 min; (2) responds to relatively bright light, having a dynamic range almost entirely outside the sensitivity of rods; (3) acts on the cone pathway primarily through a local retinal mechanism; and (4) detects light via an opsin:vitamin A photopigment (lambda(max) approximately 483 nm). CONCLUSIONS: A photopigment with a spectral sensitivity profile quite different from those of the classical rod and cone opsins but matching the standard profile of an opsin:vitamin A-based pigment drives adaptations of the human primary cone visual pathway according to time of day.     

Ommatidial structure in relation to turnover of photoreceptor membrane in the locust

Summary In the compound eye of the locust, Locusta, the cross-sectional area of the rhabdoms increases at dusk by 4.7-fold due to the rapid assembly of new microvillar membrane, and decreases at dawn by a corresponding amount as a result of pinocytotic shedding from the microvilli. The rhabdoms at night have more and longer photoreceptor microvilli than rhabdoms during the day. The orientations of the six rhabdomeres that comprise the distal rhabdom also change. The density of intramembrane particles on the P-face of the microvillar membrane, putatively representing mostly rhodopsin molecules, or aggregates thereof, does not change.An alteration in the size of the ommatidial field-stop, produced by the primary pigment cells, is concomitant with the change in rhabdom size. At night the increase in size of the field-stop must widen the angular acceptance of a rhabdom, increasing the capture of photons from an extended field. Conversely, during the day, when photons are more abundant, its decrease must narrow the acceptance angle, increasing angular resolution. Because of the presence of this field-stop, the optics of the ommatidium would not be greatly affected if the rhabdom were to remain always at its night size. It is argued, therefore, that the variable-size rhabdom must have resulted from some demand other than that of light/dark adaptation.Changes in size and organisation of the rhabdoms in response to various light regimes indicate that: (1) Rapid shedding of photoreceptor membrane is induced by the onset of light, but shedding also occurs slowly in darkness during the day. (2) Microvillar assembly is initiated by the onset of darkness, but also occurs at the normal time of dusk without a change in ambient lighting, provided there has been some light during the day. Therefore, both shedding and assembly of microvillar membrane are affected by the state of illumination, but also appear to be under some endogenous control.     

The eye of the freshwater prosobranch gastropod Viviparus viviparus: ultrastructure, electrophysiology and behaviour

We used light and electron microscopy to study the retinal organization of the eye of Viviparus viviparus. Electroretinogram (ERG) recordings were used to investigate the electrophysiological responsiveness to flashes of light of varying intensity and colour, behavioural observations were made of phototactic reactions, and optical measurements and calculations related to the path of light rays in the eye were made. The retina contains principally two types of cells: first, photoreceptor cells with both microvilli and cilia, and second, cells, often strongly pigmented, that are supportive in nature. The ERGs obtained were essentially similar in form, amplitude and duration to those known from other gastropods that have exclusively rhabdomeric photoreceptors. Spectral sensitivity curves closely fitted the absorption spectrum of a rhodopsin‐like pigment. The spectral sensitivity peak was at 475 nm. Measurements of the refractive indices of the lens gave values of 1.55 for the outer layer and 1.57 for the lens core. None of the snails tested exhibited a ‘defensive reflex’ and although no preference between light and dark regions was expressed, we nevertheless argue that, on the basis of optical measurements and calculations, the eye of V. viviparus is well‐adapted for seeing under water. Our main conclusion is that in the eye of V. viviparus with its ‘mixed photoreceptor’ cell type, there is an equal probability for microvilli and cilia to function as principal photoreceptive elements.     

BRAIN PHOTORECEPTOR PATHWAYS CONTRIBUTING TO CIRCADIAN RHYTHMICITY IN CRAYFISH

Freshwater crayfish have three known photoreceptive systems: the compound eyes, extraretinal brain photoreceptors, and caudal photoreceptors. The primary goal of the work described here was to explore the contribution of the brain photoreceptors to circadian locomotory activity and define some of the underlying neural pathways. Immunocytochemical studies of the brain photoreceptors in the parastacid (southern hemisphere) crayfish Cherax destructor reveal their expression of the blue light-sensitive photopigment cryptochrome and the neurotransmitter histamine. The brain photoreceptors project to two small protocerebral neuropils, the brain photoreceptor neuropils (BPNs), where they terminate among fibers expressing the neuropeptide pigment-dispersing hormone (PDH), a signaling molecule in arthropod circadian systems. Comparable pathways are also described in the astacid (northern hemisphere) crayfish Procambarus clarkii. Despite exhibiting markedly different diurnal locomotor activity rhythms, removal of the compound eyes and caudal photoreceptors in both C. destructor and P. clarkii (leaving the brain photoreceptors intact) does not abolish the normal light/dark activity cycle in either species, nor prevent the entrainment of their activity cycles to phase shifts of the light/dark period. These results suggest, therefore, that crayfish brain photoreceptors are sufficient for the entrainment of locomotor activity rhythms to photic stimuli, and that they can act in the absence of the compound eyes and caudal photoreceptors. We also demonstrate that the intensity of PDH expression in the BPNs varies in phase with the locomotor activity rhythm of both crayfish species. Together, these findings suggest that the brain photoreceptor cells can function as extraretinal circadian photoreceptors and that the BPN represents part of an entrainment pathway synchronizing locomotor activity to environmental light/dark cycles, and implicating the neuropeptide PDH in these functions. (Author correspondence: bbeltz@wellesley.edu)