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.

Cobalt ions inhibit negative feedback in the outer retina by blocking hemichannels on horizontal cells

2004 ◽  
Vol 21 (4) ◽  
pp. 501-511 ◽  
Author(s):  
I. FAHRENFORT ◽  
T. SJOERDSMA ◽  
H. RIPPS ◽  
M. KAMERMANS
Keyword(s):  
Negative Feedback ◽  
Glutamate Release ◽  
Horizontal Cell ◽  
Activation Function ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Small Shift ◽  
Cobalt Ions ◽  
Low Concentrations ◽  
Spectral Coding

In goldfish, negative feedback from horizontal cells to cones shifts the activation function of the Ca2+ current of the cones to more negative potentials. This shift increases the amount of Ca2+ flowing into the cones, resulting in an increase in glutamate release. The increased glutamate release forms the basis of the feedback-mediated responses in second-order neurons, such as the surround-induced responses of bipolar cells and the spectral coding of horizontal cells. Low concentrations of Co2+ block these feedback-mediated responses in turtle retina. The mechanism by which this is accomplished is unknown. We studied the effects of Co2+ on the cone/horizontal network of goldfish retina and found that Co2+ greatly reduced the feedback-mediated responses in both cones and horizontal cells in a GABA-independent way. The reduction of the feedback-mediated responses is accompanied by a small shift of the Ca2+ current of the cones to positive potentials. We have previously shown that hemichannels on the tips of the horizontal cell dendrites are involved in the modulation of the Ca2+ current in cones. Both the absence of this Co2+-induced shift of the Ca2+ current in the absence of a hemichannel conductance and the sensitivity of Cx26 hemichannels to low concentrations of Co2+ are consistent with a role for hemichannels in negative feedback from horizontal cells to cones.

scholarly journals Intrinsic Cone Adaptation Modulates Feedback Efficiency from Horizontal Cells to Cones

1999 ◽  
Vol 114 (4) ◽  
pp. 511-524 ◽  
Author(s):  
I. Fahrenfort ◽  
R.L. Habets ◽  
H. Spekreijse ◽  
M. Kamermans
Keyword(s):  
Membrane Potential ◽  
Time Constant ◽  
Calcium Current ◽  
Horizontal Cell ◽  
Light Response ◽  
Horizontal Cells ◽  
Spectral Processing ◽  
Kinetics Of ◽  
Feedback Pathway ◽  
Cone Adaptation

Processing of visual stimuli by the retina changes strongly during light/dark adaptation. These changes are due to both local photoreceptor-based processes and to changes in the retinal network. The feedback pathway from horizontal cells to cones is known to be one of the pathways that is modulated strongly during adaptation. Although this phenomenon is well described, the mechanism for this change is poorly characterized. The aim of this paper is to describe the mechanism for the increase in efficiency of the feedback synapse from horizontal cells to cones. We show that a train of flashes can increase the feedback response from the horizontal cells, as measured in the cones, up to threefold. This process has a time constant of ∼3 s and can be attributed to processes intrinsic to the cones. It does not require dopamine, is not the result of changes in the kinetics of the cone light response and is not due to changes in horizontal cells themselves. During a flash train, cones adapt to the mean light intensity, resulting in a slight (4 mV) depolarization of the cones. The time constant of this depolarization is ∼3 s. We will show that at this depolarized membrane potential, a light-induced change of the cone membrane potential induces a larger change in the calcium current than in the unadapted condition. Furthermore, we will show that negative feedback from horizontal cells to cones can modulate the calcium current more efficiently at this depolarized cone membrane potential. The change in horizontal cell response properties during the train of flashes can be fully attributed to these changes in the synaptic efficiency. Since feedback has major consequences for the dynamic, spatial, and spectral processing, the described mechanism might be very important to optimize the retina for ambient light conditions.

scholarly journals Evidence that Exocytosis Is Driven by Calcium Entry Through Multiple Calcium Channels in Goldfish Retinal Bipolar Cells

2009 ◽  
Vol 101 (5) ◽  
pp. 2601-2619 ◽  
Author(s):  
Michael Coggins ◽  
David Zenisek
Keyword(s):  
Membrane Potential ◽  
Calcium Channels ◽  
Neurotransmitter Release ◽  
Action Potentials ◽  
Bipolar Cells ◽  
Neural Cells ◽  
Dependent Manner ◽  
Vesicle Release ◽  
Calcium Dependent ◽  
Cell Capacitance

Ribbon-containing neurons represent a subset of neural cells that undergo graded membrane depolarizations rather than Na+-channel evoked action potentials. Bipolar cells of the retina are one type of ribbon-containing neuron and extensive research has demonstrated kinetically distinct pools of vesicles that are released and replenished in a calcium-dependent manner. In this study, we look at the properties of the fastest pool of releasable vesicles in these cells, often referred to as the immediately releasable pool (IRP), to investigate the relationships between vesicle release and calcium channels in these terminals. Using whole cell capacitance measurements, we monitored exocytosis in response to different magnitude and duration depolarizations, with emphasis on physiologically relevant step depolarizations. We find that release rate of the IRP increases superlinearly with membrane potential and that the IRP is sensitive to elevated EGTA concentrations in a membrane-potential–dependent manner across the physiological range of membrane potentials. Our results are best explained by a model in which multiple Ca2+ channels act in concert to drive exocytosis of a single synaptic vesicle. Pooling calcium entering through many calcium channels may be important for reducing stochastic noise in neurotransmitter release associated with the opening of individual calcium channels.

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.

Excitatory amino acid receptors of rod- and cone-driven horizontal cells in the rabbit retina

1987 ◽  
Vol 57 (3) ◽  
pp. 645-659 ◽  
Author(s):  
S. C. Massey ◽  
R. F. Miller
Keyword(s):  
Membrane Potential ◽  
Amino Acid ◽  
Excitatory Amino Acid ◽  
Direct Action ◽  
Horizontal Cell ◽  
Nmda Antagonist ◽  
Horizontal Cells ◽  
Rabbit Retina ◽  
Light Responses ◽  
Axon Terminals

Intracellular recordings were obtained from horizontal cells in the superfused retina-eyecup preparation of the rabbit. Rod- and cone-dominated horizontal cells were studied using bath-applied excitatory amino acid analogues. Cone-dominated horizontal cell somas were depolarized by kainate (KA) or quisqualate (QQ) and their light responses were reduced or abolished. They were not affected by N-methyl-DL-aspartate (NMDLA) at concentrations up to 2 mM or by 2-amino-4-phosphonobutyrate (APB), a selective agonist for the ON bipolar cell. When synaptic transmission was blocked with cobalt, horizontal cell somas were hyperpolarized. Under these conditions, KA and QQ caused large depolarizations suggesting that these agents have a direct action on horizontal cell somas. Excitatory amino acid antagonists such as cis-2,3-piperidine dicarboxylic acid (PDA) and kynurenic acid (Kyn) hyperpolarized horizontal cell somas to the level of the light-driven membrane potential. These antagonists blocked both the light-driven responses and the depolarizing action of KA. The specific NMDA antagonist 2-amino-7-phosphonoheptanoate (AP-7) had no effect on the membrane potential or light-driven responses of horizontal cell somas. In contrast to a previous report, we found no evidence that low concentrations of NMDLA could hyperpolarize horizontal cells or act as a KA antagonist in the rabbit retina. Rod-dominated axon terminals were identified by waveform, threshold, and the presence of a large rod after-potential evoked by high light intensity. These cells were depolarized by KA and their light responses were attenuated. NMDLA and APB had no effect on these cells. The general antagonists, PDA and Kyn, hyperpolarized axon terminals and blocked their light-evoked responses. The specific NMDA antagonist, AP-7, had no effect on these cells. These results suggest that the synaptic receptors that mediate light input to both rod- and cone-dominated horizontal cells are kainate or quisqualate receptors. This implies that the rod and cone transmitters of the rabbit retina are similar, with the characteristics of an excitatory amino acid, such as glutamate.

scholarly journals Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina

1993 ◽  
Vol 13 (7) ◽  
pp. 2898-2909 ◽  
Author(s):  
M Tachibana ◽  
T Okada ◽  
T Arimura ◽  
K Kobayashi ◽  
M Piccolino
Keyword(s):  
Neurotransmitter Release ◽  
Calcium Current ◽  
Bipolar Cells ◽  
Goldfish Retina

Different types of synapses with different spectral types of cones underlie color opponency in a bipolar cell of the turtle retina

1999 ◽  
Vol 16 (5) ◽  
pp. 801-809 ◽  
Author(s):  
SILKE HAVERKAMP ◽  
WOLFGANG MÖCKEL ◽  
JOSEF AMMERMÜLLER
Keyword(s):  
Bipolar Cell ◽  
Metabotropic Glutamate Receptors ◽  
Horizontal Cell ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Color Processing ◽  
Ionotropic Receptors ◽  
Metabotropic Glutamate ◽  
Different Types ◽  
Color Opponency

Electrophysiologically, color-opponent retinal bipolar cells respond with opposite polarities to stimulation with different wavelengths of light. The origin of these different polarities in the same bipolar cell has always been a mystery. Here we show that an intracellularly recorded and HRP-injected, red-ON, blue/green-OFF bipolar cell of the turtle retina made invaginating (ribbon associated) synapses exclusively with L-cones. Non-invaginating synapses resembling wide-cleft basal junctions were made exclusively with M-cones. Input from S-cones was not seen. From these results we suggest sign-inverting transmission from L-cones at invaginating synapses via metabotropic glutamate receptors, and sign-conserving transmission from M-cones at wide-cleft basal junctions via ionotropic receptors. To explain the pronounced blue sensitivity of the bipolar cell, computer simulations were performed using a sign-conserving input from a yellow/blue chromaticity-type (H3) horizontal cell. The response properties of the red-ON, blue/green-OFF bipolar cell could be quantitatively reproduced by this means. The simulation also explained the asymmetry in L- and M-cone inputs to the bipolar cell as found in the ultrastructural analysis and assigned a putative role to H3 horizontal cells in color processing in the turtle retina.

Contribution of rod, on-bipolar, and horizontal cell light responses to the ERG of dogfish retina

1999 ◽  
Vol 16 (3) ◽  
pp. 503-511 ◽  
Author(s):  
R.A. SHIELLS ◽  
G. FALK
Keyword(s):  
Bipolar Cell ◽  
Time Course ◽  
Horizontal Cell ◽  
Full Range ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Negative Wave ◽  
Low Light ◽  
Cell Responses ◽  
Light Intensities

Simultaneous extracellular ERG and intracellular recordings from horizontal and ON-bipolar cells were obtained from the dark-adapted retina of the dogfish. The light intensity–peak response relation (IR) and time course of on-bipolar cell responses closely resembled that of the ERG b-wave, but only at low light intensities [<10 rhodopsin molecules bleached per rod (Rh*)]. Block of on-bipolar cell responses with 50 μM 2-amino-4-phosphonobutyrate (APB) abolished the b-wave and unmasked a vitreal-negative wave. Subtraction from the control ERG resulted in the isolation of a vitreal-positive ERG with an IR which matched that of on-bipolar cells over the full range of light intensities. The D.C. component of the ERG arises as a result of sustained depolarization of on-bipolar cells in response to long (>0.5 s) dim light stimuli, or following bright light flashes. The IR of horizontal cells and the vitreal-negative wave unmasked by APB could be matched by scaling at low light intensities (<5 Rh*). However, horizontal cell responses saturated at about 30 Rh*, while the vitreal-negative wave continued to increase in amplitude. The time course of horizontal cell membrane current with dim flashes could be matched to the rising phase of the vitreal-negative wave, assuming that the delay in generating the voltage response in horizontal cells is due to their long (100 ms) membrane time constant. Blocking post-photoreceptor activity resulted in a much smaller vitreal-negative wave than that unmasked by APB alone. We conclude that the b-wave arises from on-bipolar cell depolarization, while the leading edge of the a-wave is a composite of the change in extracellular voltage drop across the rod layer and a component (proximal PIII) reflecting a decrease in extracellular K+ as horizontal cell synaptic channels close with light.

scholarly journals Analyses of bipolar cell responses elicited by polarization of horizontal cells.

1982 ◽  
Vol 79 (1) ◽  
pp. 131-145 ◽  
Author(s):  
J Toyoda ◽  
T Kujiraoka
Keyword(s):  
Bipolar Cell ◽  
Horizontal Cell ◽  
Bipolar Cells ◽  
Horizontal Cells ◽  
Na Channels ◽  
Cell Responses ◽  
Ionic Mechanisms ◽  
Cl Channels ◽  
Hyperpolarizing Response ◽  
Conductance Changes

Simultaneous intracellular recordings were made from a bipolar cell and a horizontal cell in the carp retina. The properties of the bipolar cell were studied while injecting current into the horizontal cell. Hyperpolarization of horizontal cells, irrespective of their type, elicited a hyperpolarizing response in on-center bipolar cells and a depolarizing response in off-center bipolar cells. Analyses of the ionic mechanisms of bipolar cell responses revealed that depolarization of horizontal cells simulated and hyperpolarization opposed the effect of central illumination. The effect of polarization was exerted in such a manner that each type of horizontal cells modified the transmission from those photoreceptors from which they receive main inputs. In on-center bipolar cells, for example, the L-type horizontal cells receiving inputs mainly from red cones modified the cone-bipolar transmission accompanied by a conductance change of K+ and/or Cl- channels, and the intermediate horizontal cells receiving inputs from rods modified the rod-bipolar transmission accompanied by a conductance change of Na+ channels. In off-center bipolar cells, the effect of polarization of any type of horizontal cells was mediated mainly by conductance changes of Na+ channels. Feedback mechanisms from horizontal cells to photoreceptors could explain these results reasonably well.

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