Contrast encoding in retinal bipolar cells: Current vs. 
voltage

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.

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

Visual Neuroscience ◽

10.1017/s0952523801184087 ◽

2001 ◽

Vol 18 (4) ◽

pp. 581-597 ◽

Cited By ~ 9

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.

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Retinal bipolar cells: Temporal filtering of signals from cone photoreceptors

Visual Neuroscience ◽

10.1017/s0952523807070630 ◽

2007 ◽

Vol 24 (6) ◽

pp. 765-774 ◽

Cited By ~ 14

Author(s):

DWIGHT A. BURKHARDT ◽

PATRICK K. FAHEY ◽

MICHAEL A. SIKORA

Keyword(s):

Light Adaptation ◽

Transfer Functions ◽

Temporal Dynamics ◽

Light Flash ◽

Common Factor ◽

Bipolar Cells ◽

Human Vision ◽

Voltage Response ◽

Cone Voltage ◽

Low Pass

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.

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

Visual Neuroscience ◽

10.1017/s0952523806231043 ◽

2006 ◽

Vol 23 (1) ◽

pp. 35-47 ◽

Cited By ~ 16

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.

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Contrast Enhancement and Distributed Encoding by Bipolar Cells in the Retina

Journal of Neurophysiology ◽

10.1152/jn.1998.80.3.1070 ◽

1998 ◽

Vol 80 (3) ◽

pp. 1070-1081 ◽

Cited By ~ 20

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.

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Heterogeneous expression of voltage-dependent Na+ and K+ channels in mammalian retinal bipolar cells

Visual Neuroscience ◽

10.1017/s0952523805222010 ◽

2005 ◽

Vol 22 (2) ◽

pp. 119-133 ◽

Cited By ~ 24

Author(s):

YU-PING MA ◽

JINJUAN CUI ◽

ZHUO-HUA PAN

Keyword(s):

Membrane Potential ◽

Bipolar Cells ◽

Voltage Response ◽

Isolated Cells ◽

Voltage Dependent ◽

Negative Membrane Potential ◽

Heterogeneous Expression ◽

Retinal Bipolar Cells ◽

Rod Bipolar Cells ◽

Cone Bipolar Cells

Retinal bipolar cells show heterogeneous expression of voltage-dependent Na+ and K+ currents. We used whole-cell patch-clamp recordings to investigate the possible roles of these currents in the response properties of bipolar cells in rats. Isolated bipolar cells showed robust spontaneous regenerative activity, but the regenerative potential of rod bipolar cells reached a more depolarized level than that of cone bipolar cells. In both isolated cells and cells in retinal slices, the membrane depolarization evoked by current injection was apparently capped. The evoked membrane potential was again more depolarized in rod bipolar cells than in cone bipolar cells. Application of tetraethylammonium and 4-aminopyridine shifted the spontaneous regenerative potential as well as the evoked potential to a more depolarized level. In addition, a subclass of cone bipolar cells showed a prominent spike in the initial phase of the voltage response when the cells were depolarized from a relatively negative membrane potential. The spike was mediated mainly by tetrodotoxin-sensitive Na+ current. The presence of the spike sped up the response kinetics and enhanced the peak membrane potential. Results of this study raise the possibility that voltage-dependent K+ currents may play a role in defining different membrane operating ranges of rod and cone bipolar cells and that voltage-dependent Na+ currents may enhance the response kinetics and amplitude of certain cone bipolar cells.

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Faculty Opinions recommendation of Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1012401.185362 ◽

2003 ◽

Author(s):

Erwin Neher

Keyword(s):

Bipolar Cells ◽

Synaptic Terminal ◽

Bulk Membrane ◽

Retinal Bipolar Cells

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Faculty Opinions recommendation of Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1090998.544370 ◽

2007 ◽

Author(s):

Jens Rettig

Keyword(s):

Bipolar Cells ◽

Active Zones ◽

Retinal Bipolar Cells

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Subcellular Localization and Complements of GABAA and GABAC Receptors on Bullfrog Retinal Bipolar Cells

Journal of Neurophysiology ◽

10.1152/jn.2000.84.2.666 ◽

2000 ◽

Vol 84 (2) ◽

pp. 666-676 ◽

Cited By ~ 37

Author(s):

Jiu-Lin Du ◽

Xiong-Li Yang

Keyword(s):

Subcellular Localization ◽

Receptor Antagonist ◽

Gaba Receptor ◽

Drug Application ◽

Bipolar Cells ◽

Visual Signals ◽

Receptor Subtypes ◽

Inner Retina ◽

Axon Terminals ◽

Retinal Bipolar Cells

γ-Aminobutyric acid (GABA) receptors on retinal bipolar cells (BCs) are highly relevant to spatial and temporal integration of visual signals in the outer and inner retina. In the present work, subcellular localization and complements of GABAA and GABACreceptors on BCs were investigated by whole cell recordings and local drug application via multi-barreled puff pipettes in the bullfrog retinal slice preparation. Four types of the BCs (types 1–4) were identified morphologically by injection of Lucifer yellow. According to the ramification levels of the axon terminals and the responses of these cells to glutamate (or kainate) applied at their dendrites, types 1 and 2 of BCs were supposed to be off type, whereas types 3 and 4 of BCs might be on type. Bicuculline (BIC), a GABAA receptor antagonist, and imidazole-4-acetic acid (I4AA), a GABAC receptor antagonist, were used to distinguish GABA receptor-mediated responses. In all BCs tested, not only the axon terminals but also the dendrites showed high GABA sensitivity mediated by both GABAA and GABACreceptors. Subcellular localization and complements of GABAA and GABAC receptors at the dendrites and axon terminals were highly related to the dichotomy of offand on BCs. In the case of off BCs, GABAA receptors were rather evenly distributed at the dendrites and axon terminals, but GABAC receptors were predominantly expressed at the axon terminals. Moreover, the relative contribution of GABAC receptors to the axon terminals was prevalent over that of GABAA receptors, while the situation was reversed at the dendrites. In the case of on BCs, GABAA and GABAC receptors both preferred to be expressed at the axon terminals; relative contributions of these two GABA receptor subtypes to both the sites were comparable, while GABAC receptors were much less expressed than GABAA receptors. GABAA, but not GABAC receptors, were expressed clusteringly at axons of a population of BCs. In a minority of BCs, I4AA suppressed the GABAC responses at the dendrites, but not at the axon terminal, implying that the GABAC receptors at these two sites may be heterogeneous. Taken together, these results suggest that GABAA and GABAC receptors may play different roles in the outer and inner retina and the differential complements of the two receptors on off and on BCs may be closely related to physiological functions of these cells.

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