Natural images and contrast encoding in bipolar cells in the retina of the land- and aquatic-phase tiger salamander

2006 ◽  
Vol 23 (1) ◽  
pp. 35-47 ◽  
Author(s):  
DWIGHT A. BURKHARDT ◽  
PATRICK K. FAHEY ◽  
MICHAEL A. SIKORA
Keyword(s):  
Bipolar Cell ◽  
Light Adaptation ◽  
Dynamic Range ◽  
Bipolar Cells ◽  
Natural Images ◽  
Cumulative Probability ◽  
Tiger Salamander ◽  
Response Curves ◽  
Efficient Coding ◽  
Contrast Response

Intracellular recordings were obtained from 57 cone-driven bipolar cells in the light-adapted retina of theland-phase(adult) tiger salamander (Ambystoma tigrinum). Responses to flashes of negative and positive contrast for centered spots of optimum spatial dimensions were analyzed as a function of contrast magnitude. On average, the contrast/response curves of depolarizing and hyperpolarizing bipolar cells in theland-phaseanimals were remarkably similar to those ofaquatic-phaseanimals. Thus, the primary retinal mechanisms mediating contrast coding in the outer retina are conserved as the salamander evolves from the aquatic to the land phase. To evaluate contrast encoding in the context of natural environments, the distribution of contrasts in natural images was measured for 65 scenes. The results, in general agreement with other reports, show that the vast majority of contrasts in nature are very small. The efficient coding hypothesis of Laughlin was examined by comparing the average contrast/response curves of bipolar cells with the cumulative probability distribution of contrasts in natural images. Efficient coding was found at 20 cd/m2but at lower levels of light adaptation, the contrast/response curves were much too shallow. Further experiments show that two fundamental physiological factors—light adaptation and the nonlinear transfer across the cone-bipolar synapse are essential for the emergence of efficient contrast coding. For both land- and aquatic-based animals, the extent and symmetry of the dynamic range of the contrast/response curves of both classes of bipolar cells varied greatly from cell to cell. This apparent substrate for distributed encoding is established at the bipolar cell level, since it is not found in cones. As a result, the dynamic range of the bipolar cell population brackets the distribution of contrasts found in natural images.

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 Center/surround organization of retinal bipolar cells: High correlation of fundamental responses of center and surround to sinusoidal contrasts

2011 ◽  
Vol 28 (3) ◽  
pp. 183-192 ◽  
Author(s):  
DWIGHT A. BURKHARDT ◽  
THEODORE M. BARTOLETTI ◽  
WALLACE B. THORESON
Keyword(s):  
Receptive Field ◽  
Maximum Amplitude ◽  
High Gain ◽  
Bipolar Cells ◽  
Ambystoma Tigrinum ◽  
Response Curves ◽  
On And Off Cells ◽  
Field Organization ◽  
Receptive Field Organization ◽  
Contrast Response

AbstractReceptive field organization of cone-driven bipolar cells was investigated by intracellular recording in the intact light-adapted retina of the tiger salamander (Ambystoma tigrinum). Centered spots and concentric annuli of optimum dimensions were used to selectively stimulate the receptive field center and surround with sinusoidal modulations of contrast at 3 Hz. At low contrasts, responses of both the center and surround of both ON and OFF bipolar cells were linear, showing high gain and thus contrast enhancement relative to cones. The contrast/response curves for the fundamental response, measured by a Fast Fourier Transform, reached half maximum amplitude quickly at 13% contrast followed by saturation at high contrasts. The variation of the normalized amplitude of the center and surround responses was remarkably similar, showing linear regression over the entire response range with very high correlations, r2 = 0.97 for both ON and OFF cells. The contrast/response curves of both center and surround for both ON and OFF cells were well fit (r2 = 0.98) by an equation for single-site binding. In about half the cells studied, the nonlinear waveforms of center and surround could be brought into coincidence by scaling and shifting the surround response in time. This implies that a nonlinearity, common to both center and surround, occurs after polarity inversion at the cone feedback synapse. Evidence from paired whole-cell recordings between single cones and OFF bipolar cells suggests that substantial nonlinearity is not due to transmission at the cone synapse but instead arises from intrinsic bipolar cell and network mechanisms. When sinusoidal contrast modulations were applied to the center and surround simultaneously, clear additivity was observed for small responses in both ON and OFF cells, whereas the interaction was strikingly nonadditive for large responses. The contribution of the surround was then greatly reduced, suggesting attenuation at the cone feedback synapse.

scholarly journals Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

2016 ◽  
Vol 115 (6) ◽  
pp. 2761-2778 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Light Adaptation ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Excitatory Input ◽  
Bipolar Cells ◽  
Visual Sensitivity ◽  
Resting Membrane Potential ◽  
Wide Range

The retina adjusts its signaling gain over a wide range of light levels. A functional result of this is increased visual acuity at brighter luminance levels (light adaptation) due to shifts in the excitatory center-inhibitory surround receptive field parameters of ganglion cells that increases their sensitivity to smaller light stimuli. Recent work supports the idea that changes in ganglion cell spatial sensitivity with background luminance are due in part to inner retinal mechanisms, possibly including modulation of inhibition onto bipolar cells. To determine how the receptive fields of OFF cone bipolar cells may contribute to changes in ganglion cell resolution, the spatial extent and magnitude of inhibitory and excitatory inputs were measured from OFF bipolar cells under dark- and light-adapted conditions. There was no change in the OFF bipolar cell excitatory input with light adaptation; however, the spatial distributions of inhibitory inputs, including both glycinergic and GABAergic sources, became significantly narrower, smaller, and more transient. The magnitude and size of the OFF bipolar cell center-surround receptive fields as well as light-adapted changes in resting membrane potential were incorporated into a spatial model of OFF bipolar cell output to the downstream ganglion cells, which predicted an increase in signal output strength with light adaptation. We show a prominent role for inner retinal spatial signals in modulating the modeled strength of bipolar cell output to potentially play a role in ganglion cell visual sensitivity and acuity.

GABA- and glycine-activated currents in the rod bipolar cell of the rabbit retina

1995 ◽  
Vol 74 (2) ◽  
pp. 856-875 ◽  
Author(s):  
M. A. Gillette ◽  
R. F. Dacheux
Keyword(s):  
Gabaa Receptor ◽  
Bipolar Cell ◽  
Reversal Potential ◽  
Outward Current ◽  
Bipolar Cells ◽  
Morphological Identification ◽  
Response Curves ◽  
Patch Clamp Technique ◽  
T Distribution ◽  
Rod Bipolar Cells

1. Voltage- and ligand-gated currents were recorded from solitary rabbit rod bipolar cells using the whole cell patch-clamp technique. The rod bipolar cell forms a single, stereotypical physiological and morphological class of cells that was easily identified from other neurons and support cells after enzymatic and mechanical dissociation from isolated retina. Protein kinase C immunoreactivity confirmed the validity of using a purely morphological identification of this cell type. 2. Voltage steps in 15-mV increments from a holding potential of -45 mV elicited a large outward current activated near -30 mV. These voltage-gated currents were eliminated by using equimolar substitutions of Cs+ and tetraethylammonium+ for K+ in the pipette, indicating that they represent a mixture of K+ currents. 3. The putative inhibitory neurotransmitters gamma-aminobutyric acid (GABA) and glycine activated inward Cl- currents when pressure-applied from pipettes placed near the axon terminals of rod bipolar cells, which were voltage-clamped at -45 mV. With changes in intracellular or extracellular Cl- concentration, the reversal potential of these ligand-gated currents changed as predicted by the Nernst equation for Cl- activity. The dose-response curves for GABA and glycine were sigmoidal with saturating concentrations of 100 and 300 microM, respectively. 4. GABA-activated currents were 1) reversibly reduced by the allosteric inhibitor picrotoxin and the competitive antagonist bicuculline; 2) potentiated by the benzodiazepine diazepam and the barbiturate barbital sodium; and 3) indistinguishable from muscimol-activated currents. There was no response to the GABAB agonist baclofen. Collectively, these data strongly suggest that the GABA-activated currents in rabbit rod bipolar cells are mediated by the GABAA receptor. This is similar to the GABA-activated currents in other mammalian rod bipolar cells. 5. Application of the conformationally restricted GABA analogue cis-4-aminocrotonic acid (CACA) failed to elicit a response, whereas the conformationally extended GABA analogue trans-4-aminocrotonic acid (TACA) elicited a response similar to that of GABA. Although bicuculline appeared to suppress the GABA-activated current slightly more than the TACA-activated current (not significant using Student's t-distribution), GABA- and TACA-activated currents were equally suppressed by picrotoxin and equally enhanced by diazepam and barbital sodium. These data, coupled with the inefficacy of CACA, argue against the existence of a GABAC-type channel in the rod bipolar cell of the rabbit and suggest that GABA and TACA were activating the same GABAA receptor-channel complex.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Dopamine D1 receptor activation reduces local inner retinal inhibition to light-adapted levels

2019 ◽  
Vol 121 (4) ◽  
pp. 1232-1243 ◽  
Author(s):  
Reece E. Mazade ◽  
Michael D. Flood ◽  
Erika D. Eggers
Keyword(s):  
Bipolar Cell ◽  
Light Adaptation ◽  
Amacrine Cells ◽  
Receptor Activation ◽  
Bipolar Cells ◽  
D1 Receptor ◽  
D1 Receptors ◽  
Local Inhibition ◽  
Local Circuits ◽  
Cone Bipolar Cells

During adaptation from dim to bright environments, changes in retinal signaling are mediated, in part, by dopamine. Dopamine is released with light and can modulate retinal receptive fields, neuronal coupling, inhibitory receptors, and rod pathway inhibition. However, it is unclear how dopamine affects inner retinal inhibition to cone bipolar cells, which relay visual information from photoreceptors to ganglion cells and are important signal processing sites. We tested the hypothesis that dopamine (D)1 receptor activation is sufficient to elicit light-adapted inhibitory changes. Local light-evoked inhibition and spontaneous activity were measured from OFF cone bipolar cells in dark-adapted mouse retinas while stimulating D1 receptors, which are located on bipolar, horizontal, and inhibitory amacrine cells. The D1 agonist SKF38393 reduced local inhibitory light-evoked response magnitude and increased response transience, which mimicked changes measured with light adaptation. D1-mediated reductions in local inhibition were more pronounced for glycinergic than GABAergic inputs, comparable with light adaptation. The effects of D1 receptors on light-evoked input were similar to the effects on spontaneous input. D1 receptor activation primarily decreased glycinergic spontaneous current frequency, similar to light adaptation, suggesting mainly a presynaptic amacrine cell site of action. These results expand the role of dopamine to include signal modulation of cone bipolar cell local inhibition. In this role, D1 receptor activation, acting primarily through glycinergic amacrine cells, may be an important mechanism for the light-adapted reduction in OFF bipolar cell inhibition since the actions are similar and dopamine is released during light adaptation. NEW & NOTEWORTHY Retinal adaptation to different luminance conditions requires the adjustment of local circuits for accurate signaling of visual scenes. Understanding mechanisms behind luminance adaptation at different retinal levels is important for understanding how the retina functions in a dynamic environment. In the mouse, we show that dopamine pathways reduce inner retinal inhibition similar to increased background luminance, suggesting the two are linked and highlighting a possible mechanism for light adaptation at an early retinal processing center.

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.

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.

Organization of the outer synaptic layer in the retina of the larval tiger Salamander

1973 ◽  
Vol 265 (872) ◽  
pp. 471-489 ◽  
Keyword(s):  
Bipolar Cell ◽  
Photoreceptor Cell ◽  
Horizontal Cell ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Tiger Salamander ◽  
Serial Sections ◽  
Rods And Cones ◽  
Cell Processes ◽  
Rod Cell

The organization of the outer synaptic layer in the salamander retina was studied electronmicroscopically in serial sections of tissue prepared by conventional techniques or stained by the method of Golgi. Rod cell pedicles make ribbon junctions on cone cell processes, and rod cell processes invaginate cone pedicles without otherwise making any specialized contact with them. Horizontal cells make ribbon and distal junctions with the photoreceptor cell pedicles; a single horizontal cell may contact both rods and cones. Bipolar cells were observed to make either ribbon or basal junctions with the photoreceptor cell pedicles; in addition, certain processes believed to belong to bipolar cells make both ribbon and basal junctions with the same or different pedicles. A single bipolar cell may make contact with both rods and cones. Horizontal cells synapse on bipolar cell dendrites and on certain unidentified processes which in turn are also presynaptic to bipolar cells. Ascending branches of these processes invaginate deeply the rod and cone pedicles without otherwise engaging them in any junction. Horizontal cell processes are linked by two kinds of junctions: close membrane appositions, and contacts analogous to the distal junctions between horizontal cells and rod pedicles.

A neural model of foveal light adaptation and afterimage formation

1997 ◽  
Vol 14 (3) ◽  
pp. 403-423 ◽  
Author(s):  
Hugh R. Wilson
Keyword(s):  
Light Adaptation ◽  
Amacrine Cell ◽  
Ganglion Cells ◽  
Horizontal Cell ◽  
Neural Model ◽  
Bipolar Cells ◽  
Light Onset ◽  
Nonlinear Dynamical ◽  
Retinal Circuitry ◽  
Contrast Response

AbstractPsychophysical research has documented the existence of three processes in light adaptation: a fast subtractive process, a divisive process that is fast at light onset and slower at light offset, and a very slow subtractive process (Hayhoe et al., 1987). In the neural model developed here, the fast subtractive process is identified with horizontal cell feedback onto cones and the divisive process with amacrine cell feedback onto bipolar cells. The very slow subtractive process is identified with the modulatory feedback circuit from amacrines via interplexiform cells to horizontal cells. A nonlinear dynamical model is developed incorporating these aspects of retinal circuitry along with both ON- and OFF-center M and P pathways. This model is shown to account for many aspects of foveal light adaptation, including negative afterimage formation, and to explain a number of the physiological differences between M and P ganglion cells, including their differing contrast-response functions.

Artistic representations: Clues to efficient coding in human vision

2011 ◽  
Vol 28 (4) ◽  
pp. 371-379 ◽  
Author(s):  
DANIEL J. GRAHAM ◽  
MING MENG
Keyword(s):  
Dynamic Range ◽  
Discrimination Performance ◽  
Stimulus Presentation ◽  
Human Vision ◽  
Natural Images ◽  
Perceptual Information ◽  
Frequency Content ◽  
Efficient Coding ◽  
Artistic Representations ◽  
Statistical Relationships

AbstractIn what ways is mammalian vision—and in particular, human vision—efficiently adapted to its ecology? We suggest that human visual artwork, which is made for the human eye, holds clues that could help answer this question. Paintings are readily perceived as representations of natural objects and scenes, yet statistical relationships between natural images and paintings are nontrivial. Although spatial frequency content is generally similar for art and natural images, paintings cannot reproduce the dynamic range of luminance in scenes. Through a variety of image manipulations designed to alter image intensity distributions and spatial contrast, we here investigate the notion that artists’ representational strategies can efficiently capture salient features of natural images, and in particular, of faces. We report that humans perform near flawless discrimination of faces and nonfaces in both paintings and natural images, even for stimulus presentation durations of 12 ms. In addition, contrast negation and up-down inversion have minimal to no effect on performance for both image types, whereas 1/f noise addition significantly affects discrimination performance for art more than for natural images. Together, these results suggest artists create representations that are highly efficient for transmitting perceptual information to the human brain.

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