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.     

Spatiotemporal frequency responses of cat retinal ganglion cells

Spatiotemporal frequency responses were measured at different levels of light adaptation for cat X and Y retinal ganglion cells. Stationary sinusoidal luminance gratings whose contrast was modulated sinusoidally in time or drifting gratings were used as stimuli. Under photopic illumination, when the spatial frequency was held constant at or above its optimum value, an X cell's responsivity was essentially constant as the temporal frequency was changed from 1.5 to 30 Hz. At lower temporal frequencies, responsivity rolled off gradually, and at higher ones it rolled off rapidly. In contrast, when the spatial frequency was held constant at a low value, an X cell's responsivity increased continuously with temporal frequency from a very low value at 0.1 Hz to substantial values at temporal frequencies higher than 30 Hz, from which responsivity rolled off again. Thus, 0 cycles X deg-1 became the optimal spatial frequency above 30 Hz. For Y cells under photopic illumination, the spatiotemporal interaction was even more complex. When the spatial frequency was held constant at or above its optimal value, the temporal frequency range over which responsivity was constant was shorter than that of X cells. At lower spatial frequencies, this range was not appreciably different. As for X cells, 0 cycles X deg-1 was the optimal spatial frequency above 30 Hz. Temporal resolution (defined as the high temporal frequency at which responsivity had fallen to 10 impulses X s-1) for a uniform field was approximately 95 Hz for X cells and approximately 120 Hz for Y cells under photopic illumination. Temporal resolution was lower at lower adaptation levels. The results were interpreted in terms of a Gaussian center-surround model. For X cells, the surround and center strengths were nearly equal at low and moderate temporal frequencies, but the surround strength exceeded the center strength above 30 Hz. Thus, the response to a spatially uniform stimulus at high temporal frequencies was dominated by the surround. In addition, at temporal frequencies above 30 Hz, the center radius increased.     

Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors

Response properties of short-type (R1-6) photoreceptors of the blowfly (Calliphora vicina) were investigated with intracellular recordings using repeated sequences of pseudorandomly modulated light contrast stimuli at adapting backgrounds covering 5 log intensity units. The resulting voltage responses were used to determine the effects of adaptational regulation on signal-to-noise ratios (SNR), signal induced noise, contrast gain, linearity and the dead time in phototransduction. In light adaptation the SNR of the photoreceptors improved more than 100-fold due to (a) increased photoreceptor voltage responses to a contrast stimulus and (b) reduction of voltage noise at high intensity backgrounds. In the frequency domain the SNR was attenuated in low frequencies with an increase in the middle and high frequency ranges. A pseudorandom contrast stimulus by itself did not produce any additional noise. The contrast gain of the photoreceptor frequency responses increased with mean illumination and the gain was best fitted with a model consisting of two second order and one double pole of first order. The coherence function (a normalized measure of linearity and SNR) of the frequency responses demonstrated that the photoreceptors responded linearly (from 1 to 150 Hz) to the contrast stimuli even under fairly dim conditions. The theoretically derived and the recorded phase functions were used to calculate phototransduction dead time, which decreased in light adaptation from approximately 5-2.5 ms. This analysis suggests that the ability of fly photoreceptors to maintain linear performance under dynamic stimulation conditions results from the high early gain followed by delayed compressive feed-back mechanisms.     

Sinusoidal and delta function responses of visual cells of the Limulus eye

Dynamic responses of visual cells of the Limulus eye to stimuli of sinusoids and narrow pulses of light superimposed on a nonzero mean level have been obtained. Amplitudes and phase angles of averaged sinusoidal generator potential are plotted with respect to frequency of intensity modulation for different mean levels of light adaptation. At frequencies above 10 CPS, generator potential amplitudes decrease sharply and phase lag angle increases. At frequencies below 1 CPS, amplitude decreases. A maximum of amplitude in the region of 1 to 2 CPS is apparent with increased mean intensity. The generator potential responses are compared with those of differential equation models. Variation of gain with mean intensity for incremental stimuli is consistent with logarithmic sensitivity of the photoreceptor. Frequency response of the photoreceptor derived from narrow pulses of light predicts the frequency response obtained with sinusoidal stimuli, and the photoreceptor is linear for small signals in the light-adapted state.     

Intracellular recordings from gecko photoreceptors during light and dark adaptation

Intracellular recordings were obtained from rods in the Gekko gekko retina and the adaptation characteristics of their responses studied during light and dark adaptation. Steady background illumination induced graded and sustained hyperpolarizing potentials and compressed the incremental voltage range of the receptor. Steady backgrounds also shifted the receptor's voltage-intensity curve along the intensity axis, and bright backgrounds lowered the saturation potential of the receptor. Increment thresholds of single receptors followed Weber's law over a range of about 3.5 log units and then saturated. Most of the receptor sensitivity change in light derived from the shift of the voltage-intensity curve, only little from the voltage compression. Treatment of the eyecup with sodium aspartate at concentrations sufficient to eliminate the beta-wave of the electroretinogram (ERG) abolished initial transients in the receptor response, possibly indicating the removal of horizontal cell feedback. Aspartate treatment, however, did not significantly alter the adaptation characteristics of receptor responses, indicating that they derive from processes intrinsic to the receptors. Dark adaptation after a strongly adapting stimulus was similarly associated with temporary elevation of membrane potential, initial lowering of the saturation potential, and shift of the voltage-intensity curve. Under all conditions of adaptation studied, small amplitude responses were linear with light intensity. Further, there was no unique relation between sensitivity and membrane potential suggesting that receptor sensitivity is controlled at least in part by a step of visual transduction preceding the generation of membrane voltage change.     

Photosynthesis in modulated light: quantitative dependence of photosynthetic enhancement on flashing rate

In order to predict the potential benefit associated with mixing devices designed to introduce periodic light modulations in dense cultures of microalgae, it is necessary to develop a quantitative understanding of the relationship between the frequency of the modulations and the resulting photosynthetic efficiency enhancement. To explore this relationship, the photosynthetic rate of cells of Phaeodactylum tricornutum from a dense steady state culture was determined as a function of modulation frequency, intensity of light received, and the proportion of the total cycle period during which the cells were illuminated. At high flash frequencies, the photosynthetic rate was determined by the average intensity received by the cells (full light intensity integration), while at low frequencies the cells responded to the instantaneous intensity (no light intensity integration). Full integration was approached asymptotically with increasing flash frequency. The frequency response could be described by a rectangular hyperbola, and the parameters of this hyperbola were nearly independent of the illumination intensity and the flash proportion. The saturation constant of the hyperbola, at which the response is one-half of the maximum, was 0.67 Hz.     

Dynamic responses of electrically coupled systems

An identified pair of electrically coupled neurons in the buccal ganglion of the freshwater snail Helisoma trivolvis is an experimentally accessible model of electrical synaptic transmission. In this investigation, electrical synaptic transmission is characterized using sinusoidal frequency (Bode) responses computed by Laplace transforms and responses to brief stimuli. The frequency response of the injected neuron shows a 20-dB/decade attenuation and a phase shift from 0 degree at low frequencies to -90 degrees at high frequencies. The response of a coupled cell shows a 40-dB/decade attenuation and a phase shift from 0 degrees at low frequencies to -180 degrees at high frequencies. A simple mathematical model of electrical synaptic transmission is described that displays each of these crucial features of the measured frequency responses. Methods are described to estimate the frequency responses of coupled systems based on presynaptic measurements. The responses of the coupled system to brief pulses of current were computed using the principle of superposition. The electrical properties of coupled systems impose a minimum delay in reaching a peak in all postsynaptic responses. The delays in the postsynaptic responses to brief stimuli are related to the electrical and anatomical parameters of coupled networks.     

Rod vision is controlled by dopamine-dependent sensitization of rod bipolar cells by GABA

Dark and light adaptation of retinal neurons allow our vision to operate over an enormous light intensity range. Here we report a mechanism that controls the light sensitivity and operational range of rod-driven bipolar cells that mediate dim-light vision. Our data indicate that the light responses of these cells are enhanced by sustained chloride currents via GABA(C) receptor channels. This sensitizing GABAergic input is controlled by dopamine D1 receptors, with horizontal cells serving as a plausible source of GABA release. Our findings expand the role of dopamine in vision from its well-established function of suppressing rod-driven signals in bright light to enhancing the same signals under dim illumination. They further reveal a role for GABA in sensitizing the circuitry for dim-light vision, thereby complementing GABA's traditional role in providing dynamic feedforward and feedback inhibition in the retina.     

S-Potentials in the Skate Retina : Intracellular recordings during light and dark adaptation

The S-potentials recorded intracellularly from the all-rod retina of the skate probably arise from the large horizontal cells situated directly below the layer of receptors. These cells hyperpolarize in response to light, irrespective of stimulus wavelength, and the responses in photopic as well as scotopic conditions were found to be subserved by a single photopigment with λ_max = 500 nm. The process of adaptation was studied by recording simultaneously the threshold responses and membrane potentials of S-units during both light and dark adaptation. The findings indicate that the sensitivity of S-units, whether measured upon steady background fields or in the course of dark adaptation, exhibits changes similar to those demonstrated previously for the ERG b-wave and ganglion cell discharge. However, the membrane potential level of the S-unit and its sensitivity to photic stimulation varied independently for all the adapting conditions tested. It appears, therefore, that visual adaptation in the skate retina occurs before the S-unit is reached, i.e., at the receptors themselves.     

Photoelectric effects in Characean cells I. The influence of light intensity

Summary The kinetic features of the action of light on the membrane potential ofNitella mucronata were investigated by measuring the frequency responses at different light intensities ranging from 0.2 to 80 W/m². Frequencies from 1 cycle/3 h to 32 cycles/min were applied. This range exceeded that of earlier investigations and resulted in the demonstration of allpass elements at low frequencies. From the all-pass elements it was concluded that the system comprises parallel pathways.From the influence of the light intensity on the frequency responses it was seen that the kinetic data depend on the intensity. By means of the Laplace transformation the squarewave responses were calculated from the frequency responses, and it could be demonstrated that a single cell is able of exhibiting all those different types of curve shapes reported in literature, if only one parameter, the light intensity, is changed. With constant modulation depth the amplitude of the evoked changes in potential varied only little with the light intensity. This is in line with a logarithmic dose-effect function as known from many light effects.     

The amplitudes of unit events in Limulus photoreceptors are modulated from an input that resembles the overall response

Light adaptation is a gain-control process that endows photoreceptors with large dynamic range. In invertebrates, this process appears to be mediated by a negative feedback that sets the amplitude of the isolated photon responses (bumps) by modulating an enzyme's rate of catalysis. This paper reports measurements of the feedback dynamics of Limulus from the responses to small modulations in light intensity. The responses show a noise that apparently arises from the random arrival of photons. We use a dynamic noiseanalysis technique to extract the cells's frequencyresponse transfer function for bump amplitude. Its ratio to the transfer function for the summed response of the cell has a simple form at low frequencies. This indicates that the origin of the feedback responsible for the adaptation is at a stage temporally close to the final conductance response. Moreover, the form of the transfer function suggests feedback by a chemical agent which is removed by a single enzymatic-like stage at low light intensity and by several such stages in parallel but with a spread of time constants at high intensity.This work was supported by grants from the Binational Science Foundation (BSF) Jerusalem, Israel and the Israel Academy of Sciences and Humanities, by NIH grant EY 1428, and by NSF grant DMS 8505442     

Color-sensitive motility and methanol release responses in Rhodobacter sphaeroides

Blue-light-induced repellent and demethylation responses, characteristic of behavioral adaptation, were observed in Rhodobacter sphaeroides. They were analyzed by computer-assisted motion analysis and through the release of volatile tritiated compounds from [methyl-(3)H]methionine-labeled cells, respectively. Increases in the stop frequency and the rate of methanol release were induced by exposure of cells to repellent light signals, such as an increase in blue- and a decrease in infrared-light intensity. At a lambda of >500 nm the amplitude of the methanol release response followed the absorbance spectrum of the photosynthetic pigments, suggesting that they function as photosensors for this response. In contrast to the previously reported motility response to a decrease in infrared light, the blue-light response reported here does not depend on the number of photosynthetic pigments per cell, suggesting that it is mediated by a separate sensor. Therefore, color discrimination in taxis responses in R. sphaeroides involves two photosensing systems: the photosynthetic pigments and an additional photosensor, responding to blue light. The signal generated by the former system could result in the migration of cells to a light climate beneficial for photosynthesis, while the blue-light system could allow cells to avoid too-high intensities of (harmful) blue light.     

The sensitivity of chlamydomonas photoreceptor is optimized for the frequency of cell body rotation.

For phototactic migration, Chlamydomonas scans the surrounding light environment by rotating the cell body with an eyespot located on the equator. The intensity of the light signal received by the eyespot should therefore change cyclically at the frequency of the cell body rotation. In this study, the response of the photoreceptor to cyclically changing light stimuli was analyzed using immotile mutant cells. To simulate the light intensity change perceived by a rotating cell, light stimuli were applied that consisted of a light phase with the intensity changing similar to a half cycle of a sine wave and a dark phase of the same length. The fluence rate at the peak of the sine wave was of the order of 10(19) photons m(-2) s(-1), i.e. high intensity at which phototaxis is saturated. A photoreceptor current (PRC) was produced at the onset of each light phase. Interestingly, its amplitude varied depending on the frequency and was largest at 1-5 Hz, a frequency range similar to the frequency of cell body rotation. Experiments on the kinetics of the PRC indicate that the response was small at low frequency because of the inactivation of the PRC before full activation. In contrast, at high frequency the PRC was suppressed by adaptation to the repetitive stimuli. These characteristic kinetics of the PRC should be important for Chlamydomonas cells to extract information from the signals generated by the cell body rotation.     

Temperature Effect on the Photo-Accumulation and Phobic Response of Volvox aureus*

SYNOPSIS. The effect of temperature on photoaccumulation and photophobic response of Volvox aureus were studied. The algae exhibited positive photoaccumulation at room temperature and negative at low temperature. When stimulated with light of intermediate intensiy (～ 5 × 10³ lux), the phobic response of the algae consisted of a decrease in the frequency or the cessation of flagellar movement in the anterior cells. At room temperature, an increase in light intensity elicited the phobic response, whereas at low temperature a decrease in light intensity was the effective stimulus. The phobic response lasted only a few seconds. The positive and negative photoaccumulations of the algae could be explained by the brief cessation of flagellar movement in the anterior cells, elicited by an increase of stimulus light at room temperature or a decrease of stimulus at low temperature.     

Spatiotemporal testing and modeling of catfish retinal neurons.

The responses of retinal neurons depend on the interaction of both temporal and spatial aspects of a light stimulus. We developed a linear spatiotemporal model of receptor and horizontal cell layers in the catfish retina based on reciprocal interactions between both layers and coupling within each. Horizontal cell transfer properties were measured experimentally using white-noise intensity modulated light spots of different diameters and were compared with analytical predictions based on the model. Good agreement was obtained with a reasonable choice of model space-constants and feedback parameters. Furthermore, the same set of parameter values determined from spot experiments enabled accurate prediction of experimental horizontal cell responses to traveling gratings. The proposed feedback connections from horizontal cells to receptors quicken the time-course of responses in both layers and sharpen receptive fields.     

背景光对图形视网膜电图空间调谐特性的影响

本工作应用背景光压抑闪光视网膜电图(FERG),考察对图形视网膜电图(PERG)的空间调谐特性的影响,并与无背景光时的结果进行比较。背景光使全屏幕闪光诱发的FERG基本压抑。在这种条件下,同屏幕的图形刺激所诱发的PERG的振幅显示一定的低空间频率衰减(LSFA)。FFT分析表明,当时间频率为3.91Hz时,PERG的二次谐波呈现十分明显的LS-FA,与无背景光时的结果吻合得很好;当时间频率为7.81Hz时,也表现出LSFA,而无背景光时则缺如。这些结果表明,无背景光时记录的PERG振幅在低空间频率区偏高确实是由于混杂有亮度特异性成分—FERG。但是,PERG振幅所显示的LSFA仍不如二次谐波那么明显,这可能是因为FERG中存在的非线性成分未为背景光所完全压抑,仍然混杂在低频区的PERG反应中。     

Effect of temperature on auditory receptor functions in bushcrickets (Orthoptera, Tettigonioidea)

By electrophysiological methods, effect of temperature on bushcricket tympanal organ functions was studied. Activity of auditory receptors was recorded intracellularly in the 5th nerve of I thoracic ganglion in Tettigonia cantans, Metrioptera roeselii, M. bicolor, Platycleis albopunctata, Pholidoptera griseoaptera, and Phaneroptera falcata. The temperature was changed in the range from 17 to 34 degrees C. Heating of the tympanal organ to 30-32 degrees C led to a decrease of impulse amplitude, shortening of their duration, an increase of sensitivity, of the burst instantaneous frequency, and of the number of impulses in responses as well as to a decrease of latent periods (LP) of receptor reaction. The optimal frequency in all studied cells did not change, although range of perceived frequencies was enlarged. The frequency threshold curve of receptors either was shifted down along the ordinate scale without changes of its shape or the thresholds at various frequencies decreased non-uniformly. Thus, the obtained data indicate the absence of changes in the frequency tuning of the auditory receptors with changes of temperature.     

Alternating electric fields stimulate ATP synthesis in Escherichia coli

External alternating electric fields of low intensity stimulated membrane bound ATP synthesis in starving Escherichia coli cells with electric field amplitudes of 2.5-50 V/cm and a frequency optimum at 100 Hz. The model of electrocon-formational coupling was used to analyze the frequency and amplitude responses of ATP synthesis. Two relaxation frequencies of the system were obtained at 44 Hz and 220 Hz, and an estimate of roughly 12 was obtained as the effective charge displacement for the catalytic cycle of ATP synthesis.     

Increased intracellular sodium mimics some but not all aspects of photoreceptor adaptation in the ventral eye of Limulus

The effects of the intracellular iontophoretic injection of Na+ ions have been quantitatively compared with adaptation in ventral photoreceptors of Limulus. We find that: (a) both light adaptation and sodium injection are associated with a decrease in the variability of the threshold response amplitued; (b) both light adaptation and sodium injection are associated with a decrease in the absolute value of the temporal dispersion of the threshold response time delay; (c) the same template curve adequately fits the intensity response relationships measured under light adaptation and Na+ injection; (d) both light adaptation and Na+ injection produce a fourfold decrease in response time delay for a desensitization of 3 log units; (e) the time coures of light adaptation and dark adaptation is significantly faster than the onset of and recovery from desensitization produced by Na+ injection; (f) unlike local illumination, Na+ injection does not produce localized desensitization of the photoreceptor. These findings suggest that a rise in intracellular Na+ concentration makes at most only a minor contribution (probably less than 5%) to the total adaptation of these receptors in the intensity range we have examined (up to 3 log units above absolute threshold). However, changes in intracellular Na+ concentration may contribute to certain components of light and dark adaptation in these receptors.     

The Adaptation of Plankton Algae IV. Light Adaptation in Different Algal Species

Two types with regard to adaptation to different light intensities are described: tbe Chlorella type and the Cyclotella type. The Chlorella type is mostly found among the green algae, the Cyclotella type among the diatoms. The Chlorella type adapts to a new light intensity mainly by changing the pigment content. Therefore the cells adapted to a high light intensity have a lower chlorophyll a content per cell than cells adapted to a low light intensity. Light saturation is mostly rather low for cells adapted to low light intensities. The light-saturated rate of photosynthesisist mostly lower for cells adapted to a high light intensity than for cells adapted to a low light intensity. The actual photosynthesis is not much higher at a high light intensity than at a low one. The actual photosynthesis is the photosynthesis at the light intensity where the cells are grown. - The Cyclotella type adapts only by changing the light-saturated rate. The chlorophyll content is the same in cells grown at low and high light intensities. Light saturation for cells grown at a low light intensity is rather high. The light-saturated rate is much higher in the case examined at the high light intensity than at the low one. The actual photosynthesis is considerably higher for cells grown at the high light intensities than for cells grown at low light intensities.- The two adaptation types are not sharply separated since transition types occur.