Effects of light adaptation on contrast processing in bipolar cells in the retina

2001 ◽  
Vol 18 (4) ◽  
pp. 581-597 ◽  
Author(s):  
PATRICK K. FAHEY ◽  
DWIGHT A. BURKHARDT
Keyword(s):  
Light Adaptation ◽  
Dynamic Range ◽  
Horizontal Cell ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Background Intensity ◽  
Ambystoma Tigrinum ◽  
Background Illumination ◽  
Voltage Range ◽  
Contrast Gain

Effects of light adaptation on contrast processing in the outer retina were investigated over nearly four decades of background illumination by analyzing the intracellular responses of 111 bipolar cells, 66 horizontal cells, and 22 cone photoreceptors in the superfused eyecup of the tiger salamander (Ambystoma tigrinum). Light adaptation had striking and similar effects on the average contrast responses of the hyperpolarizing (Bh) and depolarizing (Bd) classes of bipolar cells: Over the lower two decades of background illumination, the contrast gain increased 7-fold to reach values as high as 20–30, the dynamic range and the half-maximum contrast decreased by about 60%, the total voltage range increased some 40%, and contrast dominance changed from highly positive to more balanced. At higher levels of background, most aspects of the contrast response stabilized and Weber's Law then held closely. In this background range, the contrast gain of bipolar cells was amplified some 20× relative to that of cones whereas the corresponding amplification in horizontal cells was about 6×. Differences in the growth of contrast gain with the intensity of the background illumination for cones versus bipolar cells suggest that there are at least two adaptation-dependent mechanisms regulating contrast gain. One is evident in the cone photoresponse such that an approximately linear relation holds between the steady-state hyperpolarization and contrast gain. The other arises between the voltage responses of the cones and bipolar cells. It could be presynaptic (modulation of cone transmitter release by horizontal cell feedback or other mechanisms) and/or postsynaptic, that is, intrinsic to bipolar cells. Contrast gain grew with the background intensity by a larger factor in horizontal than in bipolar cells. This provides a basis for the widely held view that light adaptation increases the strength of surround antagonism in bipolar cells. On average, the effects of light adaptation and most quantitative indices of contrast processing were remarkably similar for Bd and Bh cells, implying that both classes of bipolar cells, despite possible differences in underlying mechanisms, are about equally capable of encoding all primary aspects of contrast at all levels of light adaptation.

Light adaptation and color opponency of horizontal cells in the turtle retina

2003 ◽  
Vol 20 (4) ◽  
pp. 437-452 ◽  
Author(s):  
GILAD TWIG ◽  
HANNA LEVY ◽  
ELITE WEINER ◽  
IDO PERLMAN
Keyword(s):  
Light Adaptation ◽  
Light Sensitivity ◽  
Horizontal Cells ◽  
Background Illumination ◽  
Voltage Range ◽  
Background Adaptation ◽  
Color Opponency ◽  
Light Stimuli ◽  
Type C

Chromaticity-type (C-type) horizontal cells of the turtle retina receive antagonistic inputs from cones of different spectral types, and therefore their response to background illumination is expected to reflect light adaptation of the cones and the interactions between their antagonistic inputs. Our goal was to study the behavior of C-type horizontal cells during background illumination and to evaluate the role of wavelength in background adaptation. The photoresponses of C-type horizontal cells were recorded intracellularly in the everted eyecup preparation of the turtleMauremys caspicaduring chromatic background illuminations. The voltage range of operation was either reduced or augmented, depending upon the wavelengths of the background and of the light stimuli, while the sensitivity to light was decreased by any background. The response–intensity curves were shifted to brighter intensities and became steeper as the background lights were made brighter regardless of wavelength. Comparing the effects of cone iso-luminant backgrounds on the Red/Green C-type horizontal cells indicated that background desensitization in these cells could not solely reflect background adaptation of cones but also depend upon response compression/expansion and changes in synaptic transmission. This leads to wavelength dependency of background adaptation in C-type horizontal cells, that is expressed as increased light sensitivity (smaller threshold elevation) and improved suprathreshold contrast detection when the wavelengths of the background and light stimuli were chosen to exert opponent effects on membrane potential.

Background-induced flicker enhancement in cat retinal horizontal cells. I. Temporal and spectral properties

1990 ◽  
Vol 64 (2) ◽  
pp. 313-325 ◽  
Author(s):  
R. Pflug ◽  
R. Nelson ◽  
P. K. Ahnelt
Keyword(s):  
Light Adaptation ◽  
Dynamic Range ◽  
Horizontal Cell ◽  
Plexiform Layer ◽  
Horizontal Cells ◽  
Enhancement Effect ◽  
Long Wavelength ◽  
Flicker Response ◽  
Response Enhancement ◽  
Cone Signal

1. Dim backgrounds can enhance small-spot flicker responses of cat retinal horizontal cells by a factor of 2 or more. 2. Intracellular marking with horseradish peroxidase (HRP) reveals that this enhancement effect occurs in--but is not necessarily limited to--the cone-connected, A-type horizontal cell. 3. Flicker amplitudes decrease over a frequency range from 3 to 36 Hz of square-wave photic stimulation. There is little evidence of flicker-response enhancement at 3 Hz. Flicker-response enhancement is typically 2-6 times larger at 35 than at 6 Hz. 4. Inspection of flicker waveforms indicates both a scaling-up of response signals with backgrounds and a distortion composed of 2- to 5-ms-latency decrease, expressed primarily within a quick component of OFF-repolarization. 5. Flicker enhancement first increases as a function of background irradiance and then decreases. The increasing limb has the dynamic range and spectral sensitivity of cat rods (507-nm peak). Enhancement is maintained during rod after-effects. The decreasing limb of the background-versus-intensity function results from light adaptation of cat, long-wavelength (red) cones. 6. The flicker responses themselves peak spectrally at approximately 555 nm and reflect only the activity of cat long-wavelength (red) cones, without evidence of intermixing of other photoreceptor mechanisms. 7. Thus within the first synaptic layer of the cat visual system, rod signals interact with the flicker responses of red cones, both increasing cone-signal amplitudes and modifying cone-signal waveforms. 8. The results are closely analogous to "suppressive rod-cone interaction" (SRCI) as described in human psychophysics. 9. An outer-plexiform-layer circuit involving rods, horizontal cells and cones may mediate rod-induced enhancement of cone flicker. This being the case, notions of horizontal-cell feedback interactions with cones may have to be modified and extended. A specific feedback model is elaborated in the companion paper.

Center-surround organization in bipolar cells: Symmetry for opposing contrasts

2003 ◽  
Vol 20 (1) ◽  
pp. 1-10 ◽  
Author(s):  
PATRICK K. FAHEY ◽  
DWIGHT A. BURKHARDT
Keyword(s):  
Bipolar Cell ◽  
Spatial Information ◽  
Horizontal Cell ◽  
Positive Contrast ◽  
Bipolar Cells ◽  
Ambystoma Tigrinum ◽  
Maximal Response ◽  
Response Curves ◽  
Contrast Polarity ◽  
Contrast Gain

Intracellular recordings were obtained from 73 cone-driven bipolar cells in the light-adapted retina of the tiger salamander (Ambystoma tigrinum). Responses to flashes of negative and positive contrast for centered spots and concentric annuli of optimum spatial dimensions were analyzed as a function of contrast magnitude. For both depolarizing and hyperpolarizing bipolar cells, it was found that remarkably similar responses were observed for the center and surround when comparisons were made between responses of the same response polarity and thus, responses to opposite contrast polarity. Thus, spatial information and contrast polarity appear to be rather strongly confounded in many bipolar cells. As a rule, the form of the contrast/response curves for center and surround approximated mirror images of each other. Contrast gain and C50 (the contrast required for half-maximal response) were quantitatively similar for center and surround when comparisons were made for responses of the same response polarity. The average contrast gain of the bipolar cell surround was 3–5 times higher than that measured for horizontal cells. Contrast/latency measurements and interactions between flashed spots and annuli showed that the surround response is delayed by 20–80 ms with respect to that of the receptive-field center. Cones showed no evidence for center-surround antagonism while for bipolar cells, the average strength of the surround ranged from about 50% to 155% of the center, depending on the test and response polarity. The results of experiments on the effects of APB (100 μM) on depolarizing bipolar cells suggest that the relative contribution of the feedback pathway (horizontal cell to cones) and the feedforward pathway (horizontal cell to bipolar cell) to the bipolar surround varies in a distributed manner across the bipolar cell population.

Physiological and pharmacological analysis of suppressive rod-cone interaction in Necturus retina [corrected]

1989 ◽  
Vol 61 (4) ◽  
pp. 866-877 ◽  
Author(s):  
T. Eysteinsson ◽  
T. E. Frumkes
Keyword(s):  
Light Adaptation ◽  
Horizontal Cell ◽  
Red Light ◽  
Background Field ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Lead Chloride ◽  
Inhibitory Influence ◽  
Third Order ◽  
Small Spot

1. Intracellular recordings were obtained from retinal neurons of the mudpuppy, Necturus, while superfusing the eyecup with various pharmacologic agents. In most experiments, the retina was continuously stimulated with a small spot of red light that was centered over the recording electrode and flickering at rates too fast for amphibian rods to follow. The retina was additionally stimulated intermittently with a dim, spatially diffuse background field of 520 nm wavelength. 2. In general, the dim background greatly enhanced flicker responsiveness. We (16) previously called this effect suppressive rod-cone interaction (SRCI) and showed it reflects a tonic suppressive influence on cone pathways that is removed by selective rod-light adaptation. 3. Lead chloride has been claimed to selectively block rod-related retinal responses (13, 35). While recording from horizontal cells lead chloride decreases responses to the dim, diffuse light flashes, enhances the frequency entrained response attributable to cones, and eliminates a background influence on flicker responses. 4. O-phospho-D-serine (DOP), kynurenic acid (KyA), and piperidine dicarboxylic acid are known to act on horizontal cells as antagonists of the photoreceptor neurotransmitter (26, 32, 33). In both depolarizing and hyperpolarizing bipolar cells, these agents enhance flicker responsiveness with no background present and prevent background enhancement of flicker. 5. Mudpuppy cones were found to have a receptive-field surround, which under our stimulus conditions is attributable to rod input. KyA, which is unknown to have any direct influence on photoreceptors, totally blocks this surround mechanism. This indicates that the cone-surround mechanism is attributable to horizontal cell feedback. The influence of KyA on SRCI in cones is similar to that observed in recordings from depolarizing bipolar cells. 6. Most sustained third-order neurons demonstrate SRCI. In these cells, SRCI is blocked by DOP or KyA. Most ON-OFF neurons fail to demonstrate SRCI under control circumstances. The ON-response of these cells is blocked by 2-amino-4-phosphonobutyric acid (31) which leaves the OFF-response intact. While their ON-response is blocked, ON-OFF neurons demonstrate SRCI. 7. The foregoing results indicate that SRCI reflects a tonic, inhibitory influence of horizontal cells on cone pathways that is removed by light-adapting rods. In part, SRCI must involve horizontal cell feedback onto cones. SRCI in third-order neurons appears to largely reflect distal retinal processing.

Effects of bicarbonate versus HEPES buffering on measured properties of neurons in the salamander retina

1998 ◽  
Vol 15 (2) ◽  
pp. 263-271 ◽  
Author(s):  
WILLIAM A. HARE ◽  
W. GEOFFREY OWEN
Keyword(s):  
Horizontal Cell ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Equilibrium Potential ◽  
Ambystoma Tigrinum ◽  
Light Responses ◽  
Internal Ph ◽  
Isolated Retina ◽  
Electrophysiological Studies ◽  
Kinetics Of

Electrophysiological studies of the isolated retina involve perfusing the tissue with a physiological Ringer's. Organic pH buffers such as HEPES have become increasingly popular in recent years because for many purposes they offer a convenient and reliable alternative to the more traditional bicarbonate/CO2. In this paper, however, we report that important functional properties of rods, bipolar cells, and horizontal cells in the salamander, Ambystoma tigrinum, are sensitive to the choice of buffer and, in the case of horizontal cells, that sensitivity is acute. In bicarbonate/CO2 Ringer's, the dark potential of the horizontal cell was typically near −50 mV and saturating light caused it to hyperpolarize to about −75 mV. On switching to HEPES-buffered Ringer's at the same pH, horizontal cells depolarized in darkness to about −20 mV, close to the chloride equilibrium potential, and the kinetics of their light responses changed. The cone-driven components of light responses increased in size relative to rod-driven components. Saturating lights still hyperpolarized the cells to −75 mV, however. Horizontal cells, being coupled via gap junctions, form a syncytium and syncytial length constants, measured in bicarbonate/CO2 Ringer's, were generally in the range 150–225 μm. On switching to HEPES-buffered Ringer's, length constants increased substantially to 250–330 μm. All these changes were reversible. We discuss our findings within the context of the cell's ability to regulate its internal pH.

Similar effects of carbachol and dopamine on neurons in the distal retina of the tiger salamander

1995 ◽  
Vol 12 (3) ◽  
pp. 443-455 ◽  
Author(s):  
William A. Hare ◽  
W. Geoffrey Owen
Keyword(s):  
Dopamine Release ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
D1 Receptors ◽  
Ambystoma Tigrinum ◽  
Tiger Salamander ◽  
Retinal Neurons ◽  
D2 Dopamine Receptors

AbstractThough there is considerable evidence that dopamine is an important retinal neuromodulator that mediates many of the changes in the properties of retinal neurons that are normally seen during light adaptation, the mechanism by which dopamine release is controlled remains poorly understood. In this paper, we present evidence which indicates that dopamine release in the retina of the tiger salamander, Ambystoma tigrinum, is driven excitatorily by a cholinergic input. We compared the effects of applying carbachol to those of dopamine application on the responses of rods, horizontal cells, and bipolar cells recorded intracellularly from the isolated, perfused retina of the tiger salamander. Micromolar concentrations of dopamine reduced the amplitudes of rod responses throughout the rods' operating range. The ratio of amplitudes of the cone-driven to rod-driven components of the responses of both horizontal and bipolar cells was increased by activation of both D1 and D2 dopamine receptors. Dopamine acted to uncouple horizontal cells and also off-center bipolar cells, the mechanism in the case of horizontal cells depending only upon activation of D1 receptors. Carbachol, a specific cholinomimetic, applied in five- to ten-fold higher concentrations, produced effects that were essentially identical to those of dopamine. These effects of carbachol were blocked by application of specific dopamine blockers, however, indicating that they are mediated secondarily by dopamine. We propose that the dopamine-releasing amacrine cells in the salamander are under the control of cells, probably amacrine cells, which secrete acetylcholine as their transmitter.

Contrast Enhancement and Distributed Encoding by Bipolar Cells in the Retina

1998 ◽  
Vol 80 (3) ◽  
pp. 1070-1081 ◽  
Author(s):  
Dwight A. Burkhardt ◽  
Patrick K. Fahey
Keyword(s):  
Contrast Enhancement ◽  
Linear Range ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Ambystoma Tigrinum ◽  
High Contrast ◽  
Cone Photoreceptors ◽  
Large Signal ◽  
Contrast Gain ◽  
Contrast Response

Burkhardt, Dwight A. and Patrick K. Fahey. Contrast enhancement and distributed encoding by bipolar cells in the retina. J. Neurophysiol. 80: 1070–1081, 1998. Responses of bipolar cells, cone photoreceptors, and horizontal cells were recorded intracellularly in superfused eyecup preparations of the tiger salamander ( Ambystoma tigrinum). Contrast flashes of positive and negative polarity were applied at the center of the receptive field while the entire retina was light adapted to a background field of 20 cd/m2. For small contrasts, many bipolar cells showed remarkably high contrast gain: up to 15–20% of the bipolar response was evoked by a contrast step of 1%. There was considerable variation from cell to cell but, on average, no striking differences in contrast gain were found between the depolarizing (Bd) and hyperpolarizing (Bh) bipolar cells. Quantitative comparisons of contrast/response measurements for cone photoreceptors and cone-driven bipolars suggest that the high contrast gain of bipolars is the consequence of a 5–10 × amplification of small signals across the cone → bipolar synapse. Bipolar cells had a very restricted linear range of response and tended to saturate at stimulus levels that were within the linear range of the cone response. The contrast/response of horizontal cells was similar to that of cones and differed markedly from that of Bh cells. For steps of equal contrast, the latency of the Bh cells was ∼20 ms shorter than that of the Bd cells regardless of the contrast magnitude. For both bipolar cells and cones, the effect of contrast polarity on latency seems largely due to the absolute value of the light step, Δ L. In the large signal domain, properties of the contrast responses of bipolar cells varied appreciably, both within and between the Bd and Bh classes. Cells of either class could be positive- or negative-contrast dominant. These and additional results show that in the light-adapted retina, the bipolar population is functionally diverse and has the potential to provide a rich substrate for distributed encoding of visual images.

Receptive field of the retinal bipolar cell: a pharmacological study in the tiger salamander

1996 ◽  
Vol 76 (3) ◽  
pp. 2005-2019 ◽  
Author(s):  
W. A. Hare ◽  
W. G. Owen
Keyword(s):  
Receptive Field ◽  
Gaba Receptors ◽  
Bipolar Cell ◽  
Horizontal Cell ◽  
Pharmacological Study ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Gaba Uptake ◽  
Gamma Aminobutyric Acid ◽  
Gabaergic Synapse

1. It is widely believed that signals contributing to the receptive field surrounds of retinal bipolar cells pass from horizontal cells to bipolar cells via GABAergic synapses. To test this notion, we applied gamma-aminobutyric acid (GABA) agonists and antagonists to isolated, perfused retinas of the salamander Ambystoma tigrinum while recording intracellularly from bipolar cells, horizontal cells, and photoreceptors. 2. As we previously reported, administration of the GABA analogue D-aminovaleric acid in concert with picrotoxin did not block horizontal cell responses or the center responses of bipolar cells but blocked the surround responses of both on-center and off-center bipolar cells. 3. Surround responses were not blocked by the GABA, antagonists picrotoxin or bicuculline, the GABAB agonist baclofen or the GABAB antagonist phaclofen, and the GABAC antagonists picrotoxin or cis-4-aminocrotonic acid. Combinations of these drugs were similarly ineffective. 4. GABA itself activated a powerful GABA uptake mechanism in horizontal cells for which nipecotic acid is a competitive agonist. It also activated, both in horizontal cells and bipolar cells, large GABAA conductances that shunted light responses but that could be blocked by picrotoxin or bicuculline. 5. GABA, administered together with picrotoxin to block the shunting effect of GABAA activation, did not eliminate bipolar cell surround responses at concentrations sufficient to saturate the known types of GABA receptors. 6. Surround responses were not blocked by glycine or its antagonist strychnine, or by combinations of drugs designed to eliminate GABAergic and glycinergic pathways simultaneously. 7. Although we cannot fully discount the involvement of a novel GABAergic synapse, the simplest explanation of our findings is that the primary pathway mediating the bipolar cell's surround is neither GABAergic nor glycinergic.

Contrast encoding in retinal bipolar cells: Current vs. voltage

2003 ◽  
Vol 20 (1) ◽  
pp. 19-28 ◽  
Author(s):  
WALLACE B. THORESON ◽  
DWIGHT A. BURKHARDT
Keyword(s):  
Dynamic Range ◽  
Linear Regression Analysis ◽  
Bipolar Cells ◽  
Response Analysis ◽  
Voltage Response ◽  
Cone Voltage ◽  
Current Response ◽  
Contrast Gain ◽  
Retinal Bipolar Cells ◽  
Contrast Response

To investigate the influence of voltage-sensitive conductances in shaping light-evoked responses of retinal bipolar cells, whole-cell recordings were made in the slice preparation of the tiger salamander, Ambystoma tigrinum. To study contrast encoding, the retina was stimulated with 0.5-s steps of negative and positive contrasts of variable magnitude. In the main, responses recorded under voltage- and current-clamp modes were remarkably similar. In general agreement with past results in the intact retina, the contrast/response curves were relatively steep for small contrasts, thus showing high contrast gain; the dynamic range was narrow, and responses tended to saturate at relatively small contrasts. For ON and OFF cells, linear regression analysis showed that the current response accounted for 83–93% of the variance of the voltage response. Analysis of specific parameters of the contrast/response curve showed that contrast gain was marginally higher for voltage than current in three of four cases, while no significant differences were found for half-maximal contrast (C50), dynamic range, or contrast dominance. In sum, the overall similarity between current and voltage responses indicates that voltage-sensitive conductances do not play a major role in determining the shape of the bipolar cell's contrast response in the light-adapted retina. The salient characteristics of the contrast response of bipolars apparently arise between the level of the cone voltage response and the postsynaptic current of bipolar cells, via the transformation between cone voltage and transmitter release and/or via the interaction between the neurotransmitter glutamate and its postsynaptic receptors on bipolar cells.

scholarly journals The Nature of Surround-Induced Depolarizing Responses in Goldfish Cones

1999 ◽  
Vol 115 (1) ◽  
pp. 3-16 ◽  
Author(s):  
D.A. Kraaij ◽  
H. Spekreijse ◽  
M. Kamermans
Keyword(s):  
Membrane Potential ◽  
Neurotransmitter Release ◽  
Calcium Current ◽  
Calcium Influx ◽  
Horizontal Cell ◽  
Activation Function ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Calcium Dependent ◽  
Postsynaptic Cell

Cones in the vertebrate retina project to horizontal and bipolar cells and the horizontal cells feedback negatively to cones. This organization forms the basis for the center/surround organization of the bipolar cells, a fundamental step in the visual signal processing. Although the surround responses of bipolar cells have been recorded on many occasions, surprisingly, the underlying surround-induced responses in cones are not easily detected. In this paper, the nature of the surround-induced responses in cones is studied. Horizontal cells feed back to cones by shifting the activation function of the calcium current in cones to more negative potentials. This shift increases the calcium influx, which increases the neurotransmitter release of the cone. In this paper, we will show that under certain conditions, in addition to this increase of neurotransmitter release, a calcium-dependent chloride current will be activated, which polarizes the cone membrane potential. The question is, whether the modulation of the calcium current or the polarization of the cone membrane potential is the major determinant for feedback-mediated responses in second-order neurons. Depolarizing light responses of biphasic horizontal cells are generated by feedback from monophasic horizontal cells to cones. It was found that niflumic acid blocks the feedback-induced depolarizing responses in cones, while the shift of the calcium current activation function and the depolarizing biphasic horizontal cell responses remain intact. This shows that horizontal cells can feed back to cones, without inducing major changes in the cone membrane potential. This makes the feedback synapse from horizontal cells to cones a unique synapse. Polarization of the presynaptic (horizontal) cell leads to calcium influx in the postsynaptic cell (cone), but due to the combined activity of the calcium current and the calcium-dependent chloride current, the membrane potential of the postsynaptic cell will be hardly modulated, whereas the output of the postsynaptic cell will be strongly modulated. Since no polarization of the postsynaptic cell is needed for these feedback-mediated responses, this mechanism of synaptic transmission can modulate the neurotransmitter release in single synaptic terminals without affecting the membrane potential of the entire cell.

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