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A moving stimulus paradigm was designed to investigate color contrast encoding in the retina. Recently, this paradigm yielded suggestive evidence for color contrast encoding in zebrafish but the significance and generality remain uncertain since the properties of color coding in the zebrafish inner retina are largely unknown. Here, the question of color contrast is pursued in the goldfish retina where there is much accumulated evidence for retinal mechanisms of color vision and opponent color-coding, in particular. Recordings of a sensitive local field potential of the inner retina, the proximal negative response, were made in the intact, superfused retina in the light-adapted state. Responses to color contrast and achromatic contrast were analyzed by comparing responses to a green moving bar on green versus red backgrounds. The quantitative form of the irradiance/response curves was distinctly different under a range of conditions in 32 retinas, thereby providing robust evidence for red–green color contrast. The color contrast is based on successive contrast, occurs in the absence of overt color opponency, and clearly differs from previous findings in the goldfish retina for simultaneous color contrast mediated by color-opponent neurons. The form of the irradiance/response curves suggests that successive color contrast is particularly important when achromatic contrast is low, as often occurs in natural environments. The present results provide a parallel with the well-known principle of human color vision, first proposed by Kirschmann as the third law of color contrast, and may also have implications for the evolution of vertebrate color vision.
The retina of the zebrafish (Danio rerio) provides an unusually favorable preparation for genetic and developmental studies of the retina. Although the retina has been studied extensively for two decades, the neuronal response of the inner retina is largely unknown. This report describes a prominent local field potential of the inner retina, the Proximal Negative Response (PNR). It is best evoked by small (100 μm) precisely positioned spots of light and is exceedingly sensitive to negative luminance contrast. The polarity, waveform, and other properties of the PNR suggest that it arises primarily from ON-OFF neurons of the proximal retina. The dominant response to negative contrast and its enhancement by light adaptation is believed due to a dominant presynaptic input from OFF bipolar cells. Color contrast was investigated by analyzing responses to a green bar moving on green versus red backgrounds. Over an intermediate range of irradiance, the response to green on red was larger than the response to green on green, thereby providing evidence for the encoding of color contrast. The present findings complement the classic principle of color contrast for human vision known as Kirschmann’s third law and bring to mind the view of Walls that color contrast may have been the driving force for the evolution of color vision in lower vertebrates. In sum, the PNR of zebrafish provides clear evidence for the encoding of color and luminance contrast in the inner retina. It exhibits the defining properties common to many other vertebrates, reinforcing the view that the zebrafish may further serve as a model for retinal function and that the PNR may provide a new approach for studies of development, genetics, and retinal degeneration in zebrafish.
Receptive 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.
Much of what is currently known about the visual response of retinal bipolar cells is based on studies of rod-dominant responses to flashes in the dark in the isolated retina. This minireview summarizes quantitative findings on contrast processing in the intact light-adapted retina based on intracellular recording from more than 400 cone-driven bipolar cells in the tiger salamander: 1) In the main, the contrast responses of ON and OFF cells are surprisingly similar, suggesting a need to refine the view that ON and OFF cells provide the selective substrates for processing of positive and negative contrasts, respectively. 2) Overall, the response is quite nonlinear, showing very high gain for small contrasts, some 10–15 times greater than that of cones, but then quickly approaches saturation for higher contrasts. 3) Under optimal conditions of light adaptation, both classes of bipolar cells show evidence for efficient coding with respect to the contrasts in natural images. 4) There is a marked diversity within both the ON and OFF bipolar cell populations and an absence of discrete subtypes. The dynamic ranges bracket the range of contrasts in nature. 5) For both ON and OFF cells, the receptive field organization shows a striking symmetry between center and surround for responses of the same polarity and thus opposite contrast polarities. 6) The latency difference between ON and OFF cells is about 30 ms, which seems qualitatively consistent with a delay due to the G-protein cascade in ON bipolar cells. 7) In sum, we report quantitative evidence for at least 11 transformations in signal processing that occur between the voltage response of cones and the voltage response of bipolar cells.
The effects of synaptic blocking agents on the antagonistic surround of the receptive field of cone photoreceptors were studied intracellular recording in the retina of hte turtle (Pseudemys scripta elegans) Illumination of a cone's receptive-field surround typically evoked a hybriid depolarizing response composed of two componests: (1) the graded synaptic feedback depolarization and (2) the prolonged depolarization a distinctive, intrinsic response of the cone. The locus of action of synaptic blocking agents was analyzed by comparing their effects on the light-evoked response of horizontal cells, the hybrid cone depolarization evoked by surround illumination, and the pure prolonged depolarization evoked by intracellular current injection.
The excitatory amino-acid antagonists, d-O-phosphoserine (DOS) and kynurenic acid (KynA), suppressed the light responses of horizontal cells and eliminated the surround-evoked, hybrid cone depolarization without affecting the prolonged depolarization evoked by current injection. Cobalt at 5–10 mM suppressed horizontal cell responses and thereby eliminated surround-evoked cone depolarizations. Cobalt (5–10 mM) also blocked the current-evoked prolonged depolarization, suggesting that the intrinsic cone mechanisms responsible for the prolonged depolarization are likely to be calcium-dependent.
Various GABA agonists and antagonists were found to have no effect on the surround-evoked depolarizations of cones. In contrast, a very low concentration of cobalt (0.5 mM) selectively suppressed the light-evoked feedback depolarization of cones without affecting horizontal cell responses or the current-evoked prolonged depolarization. Cobalt at 0.5 mM thus blocks the light-evoked action of the cone feedback synapse while sparing feedforward synaptic transmission from cones to horizontal cells. The implications of the present work for the possible neurotransmitters used at these synapses is discussed.
The influence of center-surround antagonism on light adaptation in cone photoreceptors was investigated by intracellular recording from red-sensitive cones in the retina of the turtle, Pseudemys scripta elegans. Test flashes of 0.15-mm diameter were applied at the center of background fields of 0.25-mm or 2.2-mm diameter. Immediately upon expanding the background from 0.25 to 2.2 mm, the membrane potential depolarized by about 1–4 mV. The test flash response was enhanced if the depolarization was primarily due to synaptic feedback from horizontal cells, whereas the response was attenuated if the prolonged depolarization, an intrinsic response of the cone, was the dominant source of the depolarization. After several seconds, however, only the synaptic depolarization was maintained so maintained illumination of the large background field produced an enhancement of the cone's incremental sensitivity. The enhancement was examined in detail in steady-state conditions by obtaining amplitude-intensity measurements for centered test flashes on steady background fields over a large range of intensity. The effect of the large background field at any fixed intensity was fairly well described as a vertical (upward) shift of the amplitude-intensity curve obtained on the small field. This operation constitutes a quasi-subtractive mechanism of light adaptation and might provide a basis for the sort of subtractive mechanisms inferred from psychophysical studies of human vision. The enhancement was quantified by measuring the incremental sensitivity over four decades of background illumination. The magnitude of the enhancement increased with background intensity and then tended to stabilize at higher background intensities. The maximum difference in incremental sensitivity obtained on the large vs. small background field averaged 0.46 log unit (±0.12 s.d.). At higher background intensities, incremental sensitivity conformed to Weber's Law behavior about equally well for flashes applied on either small or large background fields. In sum, the present results provide evidence for an additional mechanism of light adaptation in cone photoreceptors by showing that the incremental light sensitivity, initially set by mechanisms in the outer segment, can be modulated some three-fold by synaptic feedback at the inner segment of the cone.
Intracellular recordings were made from rods in the superfused retina of the marine toad (Bufo marinus). It was found that injection of a brief depolarizing current pulse (0.04–1 nA) evoked a distinctive, long-lasting response, here called “the prolonged depolarization.” The response appears to be regenerative, has a stereotypical waveform, is typically about 6 mV in &litude and 3 s in duration, and has a relatively long recovery period (10–60 s). As a rule, the response cannot be directly evoked by light but the current-evoked response is significantly enhanced in the presence of steady illumination. The light-evoked hyperpolarization and the depolarizing spikes of the rod are both attenuated in the presence of the prolonged depolarization. The prolonged depolarization is not an altered manifestation of the depolarizing spikes of toad rods since both can be recorded simultaneously and steady illumination suppresses the spikes while enhancing the prolonged depolarization. The response is enhanced in chloride-free superfusate and also appears to be enhanced by the use of electrodes containing chloride. The response is markedly shortened in superfusates that lack calcium or contain 1–5 mM cobalt. On this and other evidence, it is suggested that the response may be generated by the sequential action of calcium channels and calcium-activated chloride channels. Although rarely evoked by light, the prolonged depolarization of toad rods is otherwise remarkably similar to the prolonged depolarization of turtle cones. It is proposed that the prolonged depolarization, in contrast to the feedback depolarization of cones, arises from mechanisms common to both rods and cones.
The temporal dynamics of the response of neurons in the outer retina were investigated by intracellular recording from cones, bipolar, and horizontal cells in the intact, light-adapted retina of the tiger salamander (Ambystoma tigrinum), with special emphasis on comparing the two major classes of bipolars cells, the ON depolarizing bipolars (Bd) and the OFF hyperpolarizing bipolars (Bh). Transfer functions were computed from impulse responses evoked by a brief light flash on a steady background of 20 cd/m2. Phase delays ranged from about 89 ms for cones to 170 ms for Bd cells, yielding delays relative to that of cones of about 49 ms for Bh cells and 81 ms for Bd cells. The difference between Bd and Bh cells, which may be due to a delay introduced by the second messenger G-protein pathway unique to Bd cells, was further quantified by latency measurements and responses to white noise. The amplitude transfer functions of the outer retinal neurons varied with light adaptation in qualitative agreement with results for other vertebrates and human vision. The transfer functions at 20 cd/m2 were predominantly low pass with 10-fold attenuation at about 13, 14, 9.1, and 7.7 Hz for cones, horizontal, Bh, and Bd cells, respectively. The transfer function from the cone voltage to the bipolar voltage response, as computed from the above measurements, was low pass and approximated by a cascade of three low pass RC filters (“leaky integrators”). These results for cone→bipolar transmission are surprisingly similar to recent results for rod→bipolar transmission in salamander slice preparations. These and other findings suggest that the rate of vesicle replenishment rather than the rate of release may be a common factor shaping synaptic signal transmission from rods and cones to bipolar cells.
Intracellular recordings were obtained from 57 cone-driven bipolar
cells in the light-adapted retina of the land-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 the land-phase animals were remarkably similar to those
of aquatic-phase animals. 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/m2 but 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 for sinusoidal modulations of luminance contrast
was investigated by intracellular recording in the intact salamander
retina. In what appears to be the first study of this kind for
vertebrate bipolar cells, responses of the central receptive-field
mechanism of cone-driven cells to modulation of 3 Hz were analyzed
quantitatively via both signal averaging and a Fast Fourier
Transform (FFT) while the retina was light adapted to 20
cd/m2. Depolarizing and hyperpolarizing bipolar cells
showed very similar encoding. Both responded with sinusoidal waveforms
whose amplitude varied linearly with modulation depths ranging up to
7–8%. The slope of the modulation/response curve was very
steep in this range. Thus, the contrast gain was high, reaching values
of 6–7, and the half-maximal response was achieved at modulations
of 9% or less. At modulations above ∼15%, the responses typically
showed strong compressive nonlinearity and the waveform was
increasingly distorted. At maximum modulation, the higher harmonics of
the FFT constituted about 30% of the amplitude of the fundamental.
Measurements were also made for cones and horizontal cells. Both cell
types showed predominantly linear responses and low contrast gain, in
marked contrast to bipolar cells. These results suggest that the high
contrast gain and strong nonlinearity of bipolar cells largely arise
postsynaptic to cone transmitter release. Further experiments were
performed to compare responses to contrast steps versus those to
sinusoidal modulation. In the linear range, we show that the contrast
gains of cones and horizontal cells are low and virtually identical for
both steps and sinusoidal modulations. In bipolar cells, on the other
hand, the contrast gain is about two times greater for steps than that
for the 3-Hz sine waves. These results suggest that mechanisms
intrinsic to bipolar cells act like a high-pass filter with a short
time constant to selectively emphasize contrast transients over slower
changes in contrast.
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
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
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.
The impulse discharge of single ganglion cells
was recorded extracellularly in superfused eyecup preparations
of the tiger salamander (Ambystoma tigrinum).
Contrast flashes (500 ms) were applied at the center of
the receptive field while the retina was light adapted
to a background field of 20 cd/m2. The incidence
of cell types in a sample of 387 cells was: ON cells (4%),
OFF cells (28%), and ON/OFF cells (68%). Quantitative contrast/response
measurements were obtained for 83 cells. On the basis of
C50, the contrast necessary to evoke a half-maximal response,
ON/OFF cells fell into 3 groups: (1) Positive Dominant
(26%), (2) Balanced (23%), and (3) Negative Dominant (51%).
Positive Dominant cells tended to be relatively contrast
insensitive. On the other hand, many Negative Dominant
cells showed remarkably low C50 values and very steep contrast/response
curves. Contrast gain to negative contrast averaged 8.5
impulses/s/% contrast, some four times greater than that
evoked by positive contrast. In most ON/OFF cells, the
latency of the first spike evoked by a negative contrast
step was much shorter (40–100 ms) than that evoked
by a positive contrast step of equal contrast. OFF cells
typically showed higher C50 values, larger dynamic ranges,
and longer latencies than those of Negative Dominant ON/OFF
cells. Thus, different pathways or mechanism apparently
mediate the off responses of OFF and ON/OFF cells. In sum,
the light-adapted retina of the tiger salamander is strongly
biased in favor of negative contrast, as shown by the remarkably
high contrast sensitivity and faster response of Negative
Dominant cells, the remarkably low incidence of ON cells,
and the insensitivity of Positive Dominant cells. Some
possible underlying influences of bipolar and amacrine
cells are discussed.
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