Photoreceptor signaling: supporting vision across a wide range of light intensities

For decades, photoreceptors have been an outstanding model system for elucidating basic principles in sensory transduction and biochemistry and for understanding many facets of neuronal cell biology. In recent years, new knowledge of the kinetics of signaling and the large-scale movements of proteins underlying signaling has led to a deeper appreciation of the photoreceptor's unique challenge in mediating the first steps in vision over a wide range of light intensities.     

Fast negative feedback enables mammalian auditory nerve fibers to encode a wide dynamic range of sound intensities

Mammalian auditory nerve fibers (ANF) are remarkable for being able to encode a 40 dB, or hundred fold, range of sound pressure levels into their firing rate. Most of the fibers are very sensitive and raise their quiescent spike rate by a small amount for a faint sound at auditory threshold. Then as the sound intensity is increased, they slowly increase their spike rate, with some fibers going up as high as ～300 Hz. In this way mammals are able to combine sensitivity and wide dynamic range. They are also able to discern sounds embedded within background noise. ANF receive efferent feedback, which suggests that the fibers are readjusted according to the background noise in order to maximize the information content of their auditory spike trains. Inner hair cells activate currents in the unmyelinated distal dendrites of ANF where sound intensity is rate-coded into action potentials. We model this spike generator compartment as an attenuator that employs fast negative feedback. Input current induces rapid and proportional leak currents. This way ANF are able to have a linear frequency to input current (f-I) curve that has a wide dynamic range. The ANF spike generator remains very sensitive to threshold currents, but efferent feedback is able to lower its gain in response to noise.     

The stable level of coral primary production in a wide light range

Light adaptation and photosynthetic productivity were studied in common reef-building corals on islands of the Indian Ocean and the South China Sea. When light is attenuated, both in shade and at depth, adaptations by zooxanthellae permit maximal absorption and utilization of light. Better utilization of incident light in shade-dwelling and deep-water coral forms is reflected by higher values of gross photosynthesis on the plateau and linear portion of the photosynthesis-irradiance curve. It was shown that outer branches of reef-building corals are autotrophic in a major part of their light-range distribution and have a high and stable level of primary production.     

Is the membrane voltage amplifier of drone photoreceptors useful at physiological light intensities?

Free-flying drones (Apis mellifera) were attracted by pheromone to an elevated observation site where they looked for small distant objects, a visual task similar to nuptial pursuit. The brightness of the sky against which drones performed this task was measured as the radiance over a range of wavelengths covering the absorbance spectra of the principal drone rhodopsin and its metarhodopsin. This brightness varied relatively little, by just over one log unit. In laboratory experiments on the intact drone, the amplitude of photoreceptor responses to small decrements in intensity showed a marked maximum when the background intensity depolarized the cells to about –35mV. The radiance of this optimal background was only 0.2 log units greater than the sky radiance at which most drones were seen. It is argued that because of probable systematic errors the true difference may be less. It is known that in superfused retinal slices voltage-dependent sodium channels amplify small signals under these stimulus conditions. We therefore conclude that this amplification is useful for the major visual activity of the drone.     

The function of photostable pigments in fly photoreceptors

The photoreceptors in the fly's ommatidia contain a bistable visual pigment, which can be shifted back and forth by means of light of appropriate wavelengths. The situation is complicated, however, by the presence of photostable pigments. One of them (located in rhabdomeres no. 1–6) absorbs in the UV, another one (in rhabdomeres no. 7y) in the blue spectral range. Such pigments act as (dichroic) colour filters that modify the spectral and polarisation sensitivity of the photoreceptors by means of absorption. It could be shown furthermore that such pigments can also act as sensitizing pigments that modify spectral sensitivities due to sensitization.Based on material presented at the European Neurosciences Meeting, Florence, September 1978     

Influence of light intensities on dressing behavior in elderly people

With civilized environments in modern society, since the people tend to depend more on artificial illumination than on natural illumination which makes less discrepancy between day and night life, clarifying the relationship between human life and illumination is necessary. In our previous studies, we found that the subjects dressed faster with thicker clothing in the morning than in the evening when the room temperature decreased from 30 degrees C to 15 degrees C over 1 hour. We considered these results in terms of load error between the actual and set-point values in the core temperature. The present study was designed to examine the effect of bright light (3,000 lx)/dim light (50 lx) exposure (09:30 h-14:30 h) on dressing behavior and thermoregulatory responses in the elderly people during the afternoon cold exposure. Five female subjects were instructed to dress to feel comfortable when the room temperature was decreased from 30 degrees C to 15 degrees C (15:00 h-17:00 h). The subjects felt cooler and dressed more quickly with thicker clothing after dim light exposure, it is conceivable that the set-point value of core temperature is reduced under the bright light condition. We discussed these results in terms of the establishment of set-point values in the core temperature at bright light condition. If the set-point of the core temperature is lower in the bright than in the dim light condition in present experiment, the dressing behavior with thinner clothing in the bright light condition is advantageous, since it enables the core temperature to reach its set-point value more easily.     

Chemical excitation of Limulus photoreceptors. II. Vanadate, GTP-gamma- S, and fluoride prolong excitation evoked by dim flashes of light

We treated Limulus ventral photoreceptors with the phosphatase inhibitors fluoride, vanadate, and GTP-gamma-S [guanosine-5'0-(3-thiotriphosphate)] under various conditions of illumination and external calcium concentrations. In the dark in low-calcium (1 mM) artificial seawater (ASW), fluoride-induced discrete waves cluster together in time. Under these conditions, the intervals between waves were found to be correlated, and there were excess short intervals beyond the number expected from an exponential interval distribution. To assess the effects of the inhibitors on the light response, we stimulated ventral receptors with a series of dim flashes and averaged the current response under voltage clamp. In ASW, vanadate and GTP-gamma-S prolong the decay of the averaged response to dim test flashes, but prolongation does not always accompany the induction of discrete waves in the dark. Prolongation induced by vanadate in normal-calcium (10 mM) ASW was enhanced in low-calcium (1 mM Ca2+) ASW. Many individual response records suggest that prolongation results from extra discrete waves late in the light response, whereas others reveal long-lasting complex waveforms that cannot easily be resolved into discrete waves. The apparent effect of the inhibitors on the light response is to allow a single photoactivated rhodopsin molecule to produce multiple discrete waves and complex long-lasting events. We suggest that both prolongation of the light response and clustering of waves in the dark result from inhibition of a step in the pathway of visual transduction, in which GTP hydrolysis normally helps to turn off the production of both light-evoked and spontaneous waves.     

Calcitonin gene-related peptide 8-37 inhibits the evoked discharge frequency of wide dynamic range neurons in dorsal horn of the spinal cord in rats.

The present study was performed to explore the effect of calcitonin gene-related peptide 8-37 (CGRP8-37) on the electrical stimulation-evoked discharge frequency of wide dynamic range (WDR) neurons in the dorsal horn of the spinal cord in rats. The discharge frequencies of WDR neurons were evoked by transdermic electrical stimulation applied on the ipsilateral hindpaw. CGRP8-37 was applied directly on the dorsal surface of the L3 to L5 spinal cord. After the administration of 3 nmol of CGRP8-37, the evoked discharge frequency of WDR neurons decreased significantly, an effect lasting more than 30 min. The results indicate that CGRP receptors play an important role in the transmission of presumed nociceptive information in the dorsal horn of the spinal cord.     

Quantification of gene expression over a wide range by the polymerase chain reaction.

We investigated the usefulness of the polymerase chain reaction (PCR) method for the relative quantification of gene expression using a simultaneously amplified sequence of beta-actin mRNA as an internal control for the target sequence of tax/rex mRNA of human T-cell leukemia virus type I. The PCR product of the internal control was reduced by delaying the addition of the primers for its sequence. The photostimulated luminescence of the bands was measured with a laser image analyzer, and the values were plotted against the cycle number. The cycle differences between the logarithmic phase of the curves for the target sequence and for beta-actin (delta cycle) showed a linear correlation with the initial concentration of the sample. This method is highly sensitive for evaluating gene expression over a wide range.     

Cyclic GMP: control of concentration by light in retinal photoreceptors.

The cyclic GMP concentration of dark-adapted rod outer segments (ROS) is approximately 30 pmoles/mg protein and only 3 pmoles/mg protein in ROS light-adapted in vivo or in vitro. The cyclic AMP concentration of dark-adapted ROS is about 2 pmoles/mg protein with no difference observed upon bleaching. A role for cyclic GMP in the visual process may thus be indicated.     

The limited host range of an Agrobacterium tumefaciens strain extended by a cytokinin gene from a wide host range T-region

The host range of Agrobacterium tumefaciens strain LBA649 (pTiAg57) is limited to grapevine and a few other plant species. Its host range was extended through the introduction of the T-region from the wide host range octopine plasmid pTiAch5. In contrast, R prime plasmids harboring the entire wide host range virulence region were unable to achieve this effect. Via site-directed mutagenesis a search was performed to identify the T-DNA genes which were responsible for the observed host range extension. Inactivation of one of the onc-genes (the cyt gene) was found to abolish the capacity of the T-region to extend the host range of LBA649. Therefore, we cloned the cyt gene into a disarmed T-region plant vector and used it in complementation studies with pTiAg57 via the binary vector strategy. We show that the mere presence of the cyt gene from a wide host range Ti plasmid is sufficient to extend the host range of LBA649 to certain plants. We conclude that the limited host range of LBA649 is not caused by a lack of recognition of plants but is mainly due to the absence or inactivity of a cyt gene in the T-region of pTiAg57.     

Food anticipatory activity behavior of mice across a wide range of circadian and non-circadian intervals

When rodents are fed in a limited amount during the daytime, they rapidly redistribute some of their nocturnal activity to the time preceding the delivery of food. In rats, anticipation of a daily meal has been interpreted as a circadian rhythm controlled by a food-entrained oscillator (FEO) with circadian limits to entrainment. Lesion experiments place this FEO outside of the light-entrainable circadian pacemaker in the suprachiasmatic nucleus. Mice also anticipate a fixed daily meal, but circadian limits to entrainment and anticipation of more than 2 daily meals, have not been assessed. We used a video-based behavior recognition system to quantify food anticipatory activity in mice receiving 2, 3, or 6 daily meals at intervals of 12, 8, or 4-hours (h). Individual mice were able to anticipate as many as 4 of 6 daily meals, and anticipation persisted during meal omission tests. On the 6 meal schedule, pre-prandial activity and body temperature were poorly correlated, suggesting independent regulation. Mice showed a limited ability to anticipate an 18 h feeding schedule. Finally, mice showed concurrent circadian and sub-hourly anticipation when provided with 6 small meals, at 30 minute intervals, at a fixed time of day. These results indicate that mice can anticipate feeding opportunities at a fixed time of day across a wide range of intervals not previously associated with anticipatory behavior in studies of rats. The methods described here can be exploited to determine the extent to which timing of different intervals in mice relies on common or distinct neural and molecular mechanisms.     

Light acclimation maintains the redox state of the PS II electron acceptor Q2 within a narrow range over a broad range of light intensities

Chrysanthemum inducum-hybrid `Coral Charm', Hibiscus rosa-sinensis L. `Cairo Red' and Spathiphyllum wallisii Regel `Petit' were grown in natural light in a greenhouse at three levels of irradiance using permanent shade screens. Light acclimation of photosynthesis was characterized using modulated chlorophyll a fluorescence of intact leaves. A close correlation was found between the degree of reduction of the primary electron acceptor Q_A of Photosystem II (PS II) approximated as the fluorescence parameter 1−q_P, and light acclimation. The action range of 1−q_P was 0–0.4 from darkness to full irradiance around noon, within the respective light treatments in the greenhouse, indicating that most PS II reaction centres were kept open. In general, the index for electron transport (ETR) measured by chlorophyll fluorescence was higher for high-light (HL) than intermediate-(IL) and low-light (LL) grown plants. However, HL Chrysanthemum showed 40% higher ETR than HL Hibiscus at light saturation, despite identical redox states of Q_A. The light acclimation of the non-radiative dissipation of excess energy in the antenna, NPQ, varied considerably between the species. However, when normalized against q_P, a strong negative correlation was found between thermal dissipation and ETR measured by chlorophyll fluorescence. To be able to accommodate a high flux of electrons through PS II, the plants with the highest light-saturated ETR had the lowest NPQ/q_P. The possibility of using chlorophyll fluorescence for quantification of the energy balance between energy input and utilization in PS II in intact leaves is discussed. This revised version was published online in June 2006 with corrections to the Cover Date.     

The influence of extracellular calcium on the response of fly photoreceptors

Summary This paper presents a systematic investigation of the influence of the extracellular concentration of calcium ([Ca²⁺]₀) on the electrophysiological response of the fly's photoreceptors (R1–R6) to light. The hemisected heads of flies were perfused with a standard medium containing 10^–4 mol/1 CaCl₂ and in this medium the intracellularly recorded response of the cell was virtually identical to the normal response obtained in vivo. All the effects of changing the [Ca²⁺]₀ could be reversed within 5 min by perfusing the eye with the standard medium.Changing the [Ca²⁺]₀ did not influence the frequency with which quantum bumps occurred or the resting membrane potential, but did lead to changes in the latency and amplitude of the response and, most significantly, in the repolarization time (t _r). The plot oft _r versus the [Ca²⁺]₀ revealed that the value oft _r changes significantly in two distinct regions representing a [Ca²⁺]₀ of between 2×10^–8 and 10^–7 mol/l and 10^–4 and 10^–2 mol/l, respectively. Lowering the [Ca²⁺]₀ did not affect the amplitude of the response but did lead to a drastic increase int _r which was accompanied by an increase in latency and peak time. Raising the [Ca²⁺]₀ led to a reduction in the duration and amplitude of the response. The latter effect is evidence of reduction in the sensitivity of the photoreceptor cell which is dependent on the [Ca²⁺]₀.It is postulated that two types of binding site for calcium exist, high affinity binding sites (HABS) and low affinity binding sites (LABS), which modulate the functioning of ion channels in the cell membrane that are activated as a consequence of light absorption. The results indicate that the sensitivity of the photoreceptor cell is determined by the degree of saturation of the LABS.     

Desensitization of skate photoreceptors by bleaching and background light

Through extracellular measurements of photoreceptor responses to flashed stimuli, we examined how the bleaching of rhodopsin affects increment receptor threshold in the isolated retina of the skate (Raja oscellata and R. erinacea). Both initially unbleached and previously bleached photoreceptors, when exposed to full-field luminous backgrounds of fixed intensity, attain approximately stable levels of increment threshold that vary with the intensity of the background light. Values of stabilized increment thresholds measured after various extents of bleaching (less than approximately 50%), when plotted against background intensity in log-log coordinates, tend to converge with increasing intensity of the background; this relationship of the increment threshold functions resembles that which Blakemore and Rushton (1965b) found to describe the transient effect of bleaching on psychophysical increment threshold for the human rod mechanism. Our data are consistent with the possibility that related photochemical processes govern the stabilized levels of receptor sensitivity exhibited by the isolated retina (a) during steady illumination and (b) long after substantial bleaching.