Electrical coupling of retinal horizontal cells mediated by distinct voltage-independent junctions

1999 ◽  
Vol 16 (5) ◽  
pp. 811-818 ◽  
Author(s):  
CHENGBIAO LU ◽  
DAO-QI ZHANG ◽  
DOUGLAS G. McMAHON
Keyword(s):  
Single Channel ◽  
Lucifer Yellow ◽  
Horizontal Cell ◽  
Electrical Coupling ◽  
Cell Voltage ◽  
Horizontal Cells ◽  
Simultaneous Application ◽  
Dependent Inactivation ◽  
Cellular Junctions ◽  
Voltage Dependent

Electrical coupling between H2 horizontal cell pairs isolated from the hybrid bass retina was studied using dual whole-cell, voltage-clamp technique. Voltage-dependent inactivation of junctional currents in response to steps in transjunctional voltage (Vj) over a range of ±100 mV was characterized for 89 cell pairs. Approximately one-quarter of the pairs exhibited strongly voltage-dependent junctions (>50% reduction in junctional current at ±100 mV), another quarter of the pairs exhibited voltage-independent junctional current (<5% reduction at ±100 mV), and the remainder of the pairs exhibited intermediate values for voltage inactivation. We focused on further characterizing the Vj-independent junctions of horizontal cells, which have not been described previously in detail. When Lucifer Yellow dye was included in one recording pipette, pairs exhibiting Vj-independent coupling showed no (9/12), or limited (3/12), passage of dye. Vj-independent coupling was markedly less sensitive to the modulators SNP (100–300 μM, −9% reduction in coupling) and dopamine (100–300 μM, −6%) than were Vj-dependent junctions (−45% and −44%). However, simultaneous application of both SNP and dopamine significantly reduced Vj-independent coupling (−56%). Both Vj-independent and Vj-dependent junctions were blocked by DMSO (1–2%), but Vj-independent junctions were not blocked by heptanol. Single-channel junctional conductances of Vj-independent junctions range from 112–180 pS, versus 50–60 pS for Vj-dependent junctions. The results reveal that Vj-independent coupling in a subpopulation of horizontal cells from the hybrid bass retina is mediated by cellular junctions with physiological and pharmacological characteristics distinct from those previously described in fish horizontal cells.

Gap-junctional properties of electrically coupled skate horizontal cells in culture

1993 ◽  
Vol 10 (2) ◽  
pp. 287-295 ◽  
Author(s):  
Haohua Qian ◽  
Robert Paul Malchow ◽  
Harris Ripps
Keyword(s):  
Receptive Field ◽  
Lucifer Yellow ◽  
Horizontal Cell ◽  
Electrical Coupling ◽  
Cell Voltage ◽  
Horizontal Cells ◽  
Electrical Synapse ◽  
Cell Coupling ◽  
Junctional Conductance ◽  
Gap Junctional

AbstractWhole-cell voltage-clamp recordings were used to examine the unusual pharmacological properties of the electrical coupling between rod-driven horizontal cells in skate retina as revealed previously by receptive-field measurements (Qian & Ripps, 1992). The junctional resistance was measured in electrically coupled cell pairs that had been enzymatically isolated and maintained in culture; the typical value was about 19.92 MΩ(n = 45), more than an order of magnitude lower than the nonjunctional membrane resistance. These data and the intercellular spread of the fluorescent dye Lucifer Yellow provide a good indication that skate horizontal cells are well coupled. The junctional conductance between cells was not modulated by the neurotransmitters dopamine (200 μM) or GABA (1 mM), nor was it affected by the membrane-permeable analogues of cAMP or cGMP, or the adenylate cyclase activator, forskolin. Although resistant to agents that have been reported to alter horizontal-cell coupling in cone-driven horizontal cells, the junctional conductance between paired horizontal cells of skate was greatly reduced by the application of 20 mM acetate, which is known to effectively reduce intracellular pH. Together with the results obtained in situ on the receptive-field properties of skate horizontal cells, these findings indicate that the gap-junctional properties of rod-driven horizontal cells of the skate are fundamentally different from those of cone-driven horizontal cells in other species. This raises the possibility that there is more than one class of electrical synapse on vertebrate horizontal cells.

Gap junction channel gating at bass retinal electrical synapses

1996 ◽  
Vol 13 (6) ◽  
pp. 1049-1057 ◽  
Author(s):  
Chengbiao Lu ◽  
Douglas G. McMahon
Keyword(s):  
Time Constant ◽  
Time Course ◽  
Single Channel ◽  
Horizontal Cells ◽  
Electrical Synapses ◽  
Dependent Inactivation ◽  
Current Voltage ◽  
Voltage Dependent ◽  
Current Voltage Relationship ◽  
Voltage Relationship

AbstractTo further characterize the properties of retinal horizontal cell electrical synapses, we have studied the gating characteristics of gap junctions between cone-driven horizontal cells from the hybrid striped bass retina using double whole-cell voltage-clamp techniques. In a total of 105 cell pairs, the macroscopic conductance ranged from 0.4–100 nS with most cell pairs exhibiting junctional conductances between 10 and 30 nS. The junctional current-voltage relationship showed that peak or instantaneous currents (Iinst) were linear within the Vj range of ±100 mV and that steady-state junctional currents (Iss) exhibited rectification with increasing voltage beginning around ±30–40 mV Vj. The normalized junctional current-voltage relationship was well fit by a two-state Boltzmann distribution, with an effective gating charge of 1.9 charges/channel, a half-maximal voltage of approximately ±55 mV, and a normalized residual conductance of 0.28. The decay of junctional current followed a single exponential time course with the time constant decreasing with increasing Vj. Recovery of junctional current from voltage-dependent inactivation takes about 1 s following a pulse of 80 mV, and is about five times slower than the inactivation time course at the same Vj. Single-channel analysis showed that the unitary conductance of junctional channels is 50–70 pS. The overall open probability decreased in a voltage-dependent manner. Both the mean channel open time and the frequency of channel opening decreased, while the channel closure time increased. The ratio of closed time/total recording time significantly increased as Vj increased. Increased Vj reduced the number of events at all levels and shifted the unitary conductance to a lower level. Kinetic analysis of channel open duration showed that the distribution of channel open times was best fit by two exponentials and increased Vj significantly reduced the slower time constant. These results indicate that bass retina horizontal cells exhibit voltage-dependent inactivation of macroscopic junctional current. The inactivation occurs at the single-channel level mainly by increasing the rate of closure of voltage-sensitive channels.

Bifurcation analysis of nonlinear retinal horizontal cell models. II. Network properties

1990 ◽  
Vol 64 (1) ◽  
pp. 248-261 ◽  
Author(s):  
R. L. Winslow ◽  
S. Ma
Keyword(s):  
Horizontal Cell ◽  
Membrane Currents ◽  
Horizontal Cells ◽  
Synaptic Conductance ◽  
Cell Models ◽  
Voltage Dependent ◽  
Full Complement ◽  
Network Properties ◽  
Light Stimuli ◽  
Coupling Conductance

1. We have previously presented a model of horizontal-cell soma isolated from fish retina. The model consists of a synaptic conductance representing input from photoreceptors in parallel with voltage-dependent membrane currents. Membrane-current models are based on I-V curves measured in isolated fish horizontal cells. Bifurcation theory was used to analyze model properties. The major findings of this study were 1) the inward Ca2+ current must be inactivated to account for horizontal-cell resting potentials and hyperpolarizing responses to light stimuli in a background of dark, and 2) the synaptic conductance controls the bifurcation structure of the model, with bistable behavior occurring at small and monostable behavior occurring at larger values of the synaptic conductance. The synaptic conductance at the point of transition from bistable to monostable behavior corresponds to the activation of as few as 100 synaptic channels. Thus tonic synaptic input from photoreceptors and inactivation of the inward Ca2+ current act to “linearize” responses of isolated horizontal-cell models. 2. The model described in this paper extends these analyses to large networks of horizontal cells in which each cell is coupled resistively to its nearest neighbors and is modeled with the use of the full complement of nonlinear membrane currents. Network responses to arbitrary patterns of conductance change (simulating inputs from photoreceptors), current-, or voltage-clamp stimuli are computed using the Newton iteration. The Newton descent direction is computed using either conjugate gradient (CG) or preconditioned CG algorithms. 3. An analysis of network stability properties is performed. Network I-V curves are computed by voltage-clamping the center node and computing the current required to maintain the clamp voltage. Computations are performed on networks of model cells in which the Ca2+ current is fully activated and the synaptic conductance is zero, thus making each cell as nonlinear as possible. Coupling conductance values slightly greater than 100 pS provide a current shunt sufficient to prevent the generation of Ca2+ action potentials in the network. This coupling conductance corresponds to the conductance of as few as two gap-junction channels and is more than two orders of magnitude less than the coupling known to exist between pairs of cultured horizontal cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Postsynaptic Response Kinetics Are Controlled by a Glutamate Transporter at Cone Photoreceptors

1998 ◽  
Vol 79 (1) ◽  
pp. 190-196 ◽  
Author(s):  
Lubor Gaal ◽  
Botond Roska ◽  
Serge A. Picaud ◽  
Samuel M. Wu ◽  
Robert Marc ◽  
...  
Keyword(s):  
Voltage Dependence ◽  
Light Flash ◽  
Horizontal Cell ◽  
Glutamate Transporter ◽  
Light Response ◽  
Horizontal Cells ◽  
Cone Photoreceptors ◽  
Postsynaptic Response ◽  
Glutamate Concentration ◽  
Voltage Dependent

Gaal, Lubor, Botond Roska, Serge A. Picaud, Samuel M. Wu, Robert Marc, and Frank S. Werblin. Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors. J. Neurophysiol. 79: 190–196, 1998. We evaluated the role of the sodium/glutamate transporter at the synaptic terminals of cone photoreceptors in controlling postsynaptic response kinetics. The strategy was to measure the changes in horizontal cell response rate induced by blocking transporter uptake in cones with dihydrokainate (DHK). DHK was chosen as the uptake blocker because, as we show through autoradiographic uptake measurements, DHK specifically blocked uptake in cones without affecting uptake in Mueller cells. Horizontal cells depolarized from about −70 to −20 mV as the exogenous glutamate concentration was increased from ∼1 to 40 μM, so horizontal cells can serve as “glutamate electrodes” during the light response. DHK slowed the rate of hyperpolarization of the horizontal cells in a dose-dependent way, but didn't affect the kinetics of the cone responses. At 300 μM DHK, the rate of the horizontal cell hyperpolarization was slowed to only 17 ± 8.5% (mean ± SD) of control. Translating this to changes in glutamate concentration using the slice dose response curve as calibration in Fig. 2 , DHK reduced the rate of removal of glutamate from ∼0.12 to 0.031 μM/s. The voltage dependence of uptake rate in the transporter alone was capable of modulating glutamate concentration: we blocked vesicular released glutamate with bathed 20 mM Mg2+ and then added 30 μM glutamate to the bath to reestablish a physiological glutamate concentration level at the synapse and thereby depolarize the horizontal cells. Under these conditions, a light flash elicited a 17-mV hyperpolarization in the horizontal cells. When we substituted kainate, which is not transported, for glutamate, horizontal cells were depolarized but light did not elicit any response, indicating that the transporter alone was responsible for the removal of glutamate under these conditions. This suggests that the transporter was both voltage dependent and robust enough to modulate glutamate concentration. The transporter must be at least as effective as diffusion in removing glutamate from the synapse because there is only a very small light response once the transporter is blocked. The transporter, via its voltage dependence on cone membrane potential, appears to contribute significantly to the control of postsynaptic response kinetics.[Figure: see text]

The horizontal cells of artiodactyl retinae: A comparison with Cajal's descriptions

1996 ◽  
Vol 13 (4) ◽  
pp. 735-746 ◽  
Author(s):  
Daniele Sandman ◽  
Brian B. Boycott ◽  
Leo Peichl
Keyword(s):  
Sika Deer ◽  
Lucifer Yellow ◽  
Horizontal Cell ◽  
Morphological Difference ◽  
Dendritic Tree ◽  
Horizontal Cells ◽  
Important Respect ◽  
Single Axon ◽  
Familial Differences ◽  
Wild Pig

AbstractThe morphology of horizontal cells in ox, sheep, and pig retinae as observed after Lucifer Yellow injections are described and compared with the descriptions of Golgi-stained cells by Ramón y Cajal (1893). Horizontal cells in the retinae of less domesticated species, wild pig, fallow and sika deer, mouflon, and aurochs were also examined. All these retinae have two types of horizontal cell; their morphologies are in common, although with some familial differences. Their basic appearance is as Cajal described; except in one important respect, a single axon-like process could not be identified on the external horizontal cells. It is concluded that external horizontal cells of artiodactyls correspond to the axonless (A-type) cells of other mammals. Cajal's internal horizontal cells have a single axon which contacts rods. This type corresponds to the B-type cells of other mammalian retinae. Artiodactyl A- and B-type horizontal cells differ from those of many other mammals in that the B-type dendritic tree is robust and the A-type dendritic tree is delicate. Historically, this morphological difference between orders of mammals has led to some confusion. The comparisons presented here suggest that the morphological types of primate horizontal cells can be integrated into a general mammalian classification.

scholarly journals A novel action of quinine and quinidine on the membrane conductance of neurons from the vertebrate retina.

1994 ◽  
Vol 104 (6) ◽  
pp. 1039-1055 ◽  
Author(s):  
R P Malchow ◽  
H Qian ◽  
H Ripps
Keyword(s):  
Lucifer Yellow ◽  
Reversal Potential ◽  
Outward Current ◽  
Membrane Conductance ◽  
Cobalt Acetate ◽  
Cinchona Alkaloids ◽  
Horizontal Cells ◽  
Patch Clamp Technique ◽  
Voltage Dependent ◽  
Gap Junctional

The cinchona alkaloids quinine and quinidine have been shown to block a broad range of voltage-gated membrane conductances in a variety of excitable tissues. Using the whole-cell version of the patch clamp technique, we examined the effects of these compounds on voltage-dependent currents from horizontal cells dissociated enzymatically from the all-rod retina of the skate. We report here a novel and unexpected action of quinine and quinidine on isolated horizontal cells. In addition to blocking several of the voltage-activated currents of these cells, the introduction of the alkaloids evoked a large outward current when the cells were held at depolarized potentials. Using tail current analysis, the reversal potential of the outward current was close to O mV, and the current was markedly suppressed by extracellularly applied cobalt, acetate, and halothane. Depolarization in the presence of quinine also permitted entry into the cells of extracellularly applied Lucifer yellow (MW = 443 D), whereas a 3-kD fluorescein-dextran complex was excluded. These findings suggest that the large, apparently nonselective conductance induced by quinine and quinidine results from the opening of hemi-gap junctional channels.

scholarly journals Dopamine modulates in a differential fashion T- and L-type calcium currents in bass retinal horizontal cells.

1993 ◽  
Vol 102 (2) ◽  
pp. 277-294 ◽  
Author(s):  
C Pfeiffer-Linn ◽  
E M Lasater
Keyword(s):  
Cyclic Amp ◽  
Calcium Channels ◽  
Calcium Current ◽  
Horizontal Cell ◽  
Calcium Currents ◽  
Horizontal Cells ◽  
White Bass ◽  
Cell Calcium ◽  
Cone Type ◽  
Voltage Dependent

White bass (Roccus chrysops) retinal horizontal cells possess two types of voltage-activated calcium currents which have recently been characterized with regard to their voltage dependence and pharmacology (Sullivan, J., and E. M. Lasater. 1992. Journal of General Physiology. 99:85-107). A low voltage-activated transient current was identified which resembles the T-type calcium current described in a number of other preparations, along with a sustained high threshold, long-lasting calcium current that resembles the L-type calcium current. Here we report on the modulation of horizontal cell calcium channels by dopamine. Under whole-cell voltage clamp conditions favoring the expression of both calcium currents, dopamine had opposing actions on the two types of voltage-sensitive calcium currents in the same cone-type horizontal cell. The L-type calcium current was significantly potentiated by dopamine while the T-type current was simultaneously reduced. Dopamine had no effect on calcium currents in rod-type horizontal cells. Both of dopamine's actions were mimicked with the D1 receptor agonist, SKF 38393, and blocked by application of the D1 specific antagonist, SCH 23390. Dopamine's actions on the two types of calcium currents in white bass horizontal cells are mimicked by the cell membrane-permeant cyclic AMP derivative, 8-(4-chlorophenylthio)-cyclic AMP, suggesting that dopamine's action is linked to a cAMP-mediated second messenger system. Furthermore, the inhibitor of cAMP-dependent protein kinase blocked both of dopamine's actions on the voltage-dependent calcium channels when introduced through the patch pipette. This indicates that protein phosphorylation is involved in modulating horizontal cell calcium channels by dopamine. Taken together, these results show that dopamine has differential effects on the voltage-dependent calcium currents in retinal horizontal cells. The modulation of these currents may play a role in shaping the response properties of horizontal cells.

Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig

1994 ◽  
Vol 11 (3) ◽  
pp. 501-517 ◽  
Author(s):  
Leo Peichl ◽  
Juncal González-Soriano
Keyword(s):  
Guinea Pig ◽  
Calcium Binding ◽  
Ganglion Cells ◽  
Lucifer Yellow ◽  
Horizontal Cell ◽  
Cell Types ◽  
Horizontal Cells ◽  
Rodent Species ◽  
The Family ◽  
Calbindin D

AbstractRetinal horizontal cells of four rodent species, rat, mouse, gerbil, and guinea pig were examined to determine whether they conform to the basic pattern of two horizontal cell types found in other mammalian orders. Intracellular injections of Lucifer-Yellow were made to reveal the morphologies of individual cells. Immunocytochemistry with antisera against the calcium-binding proteins calbindin D-28k and parvalbumin was used to assess population densities and mosaics.Lucifer-Yellow injections showed axonless A-type and axon-bearing B-type horizontal cells in guinea pig, but revealed only B-type cells in rat and gerbil retinae. Calbindin immunocytochemistry labeled the A-and B-type populations in guinea pig, but only a homogeneous regular mosaic of cells with B-type features in rat, mouse, and gerbil. All calbindin-immunoreactive horizontal cells in the latter species were also parvalbumin-immunoreactive; comparison with Nissl-stained retinae showed that both antisera label all of the horizontal cells. Taken together, the data from cell injections and the population studies provide strong evidence that rat, mouse, and gerbil retinae have only one type of horizontal cell, the axon-bearing B-type, where as the guinea pig has both A-and B-type cells. Thus, at least three members of the family Muridae differ from other rodents and deviate from the proposed mammalian scheme of horizontal cell types.The absence of A-type cells is apparently not linked to any peculiarities in the photoreceptor populations, and there is no consistent match between the topographic distributions of the horizontal cells and those of the cone photoreceptors or ganglion cells across the four rodent species. However, the cone to horizontal cell ratio is rather similar in the species with and without A-type cells.

Whole cell and single-channel properties of a unique voltage-activated sustained calcium current identified in teleost retinal horizontal cells

1996 ◽  
Vol 75 (2) ◽  
pp. 609-619 ◽  
Author(s):  
C. L. Pfeiffer-Linn ◽  
E. M. Lasater
Keyword(s):  
Calcium Channel ◽  
Calcium Current ◽  
Single Channel ◽  
Horizontal Cell ◽  
Horizontal Cells ◽  
Unique Type ◽  
Whole Cell ◽  
White Bass ◽  
Cell Current ◽  
P Type

1. A voltage-activated, sustained calcium current in white bass retinal cone horizontal cells was characterized on the basis of electrophysiological and pharmacological criteria. Studies were performed with the use of a combination of whole cell and single-channel analysis of outside-out excised patches from isolated, cultured retinal horizontal cells. 2. We found that the white bass sustained calcium channel represents a unique type of calcium channel. On the basis of our analysis, it does not fall into any current classification scheme. The horizontal cell channel shares some biophysical and pharmacological properties with the typical high-voltage-activated L-type channel, but it also has features in common with the P-type channel. 3. The biophysical characteristics of the channel were most typical of an L-type channel. It activated above -30 mV membrane potential and only very slowly inactivated. It had a single-channel conductance of 25 pS. 4. Like the typical L-type current, the horizontal cell current was sensitive to the dihydropyridine agonist Bay K 8644. It prolonged the channel open time, which resulted in a large increase in macroscopic current flow into the cell. However, unlike the typical L current, dihydropyridine antagonists (nifedipine, nimodipine, etc.) as well as the specific L-channel inhibitor diltiazem were only moderately effective at best. 5. In a previous study, we found the current was antagonized by a factor found in funnel-web spider toxin. Here we show that the current is completely blocked by low doses of omega-agatoxin IVA. These are characteristics of the P-type calcium channel. But unlike the P current, the horizontal cell current is relatively insensitive to low or high doses of omega-conotoxin MVIIC. 6. The overall combination of calcium channel characteristics sets apart the calcium channel in bass horizontal cells from previously described channels. It appears to be a unique, tissue-specific ion channel, which we have labeled the PL channel.

Electrophysiological Properties of Mouse Horizontal Cell GABAA Receptors

2004 ◽  
Vol 92 (5) ◽  
pp. 2789-2801 ◽  
Author(s):  
Andreas Feigenspan ◽  
Reto Weiler
Keyword(s):  
Single Channel ◽  
Horizontal Cell ◽  
Chloride Ions ◽  
Horizontal Cells ◽  
Hill Coefficient ◽  
Mouse Retina ◽  
Patch Clamp Technique ◽  
Open Probability ◽  
Steady State Current ◽  
Single Channel Currents

GABA-induced currents have been characterized in isolated horizontal cells from lower vertebrates but not in mammalian horizontal cells. Therefore horizontal cells were isolated after enzymatical and mechanical dissociation of the adult mouse retina and visually identified. We recorded from horizontal cell bodies using the whole cell and outside-out configuration of the patch-clamp technique. Extracellular application of GABA induced inward currents carried by chloride ions. GABA-evoked currents were completely and reversibly blocked by the competitive GABAA receptor antagonist bicuculline (IC50 = 1.7 μM), indicating expression of GABAA but not GABAC receptors. Their affinity for GABA was moderate (EC50 = 30 μM), and the Hill coefficient was 1.3, corresponding to two GABA binding sites. GABA responses were partially reduced by picrotoxin with differential effects on peak and steady-state current values. Zinc blocked the GABA response with an IC50 value of 7.3 μM in a noncompetitive manner. Furthermore, GABA receptors of horizontal cells were modulated by extracellular application of diazepam, zolpidem, methyl 6,7-dimethoxy-4-ethyl-β-carboxylate, pentobarbital, and alphaxalone, thus showing typical pharmacological properties of CNS GABAA receptors. GABA-evoked single-channel currents were characterized by a main conductance state of 29.8 pS and two subconductance states (20.2 and 10.8 pS, respectively). Kinetic analysis of single-channel events within bursts revealed similar mean open and closed times for the main conductance and the 20.2-pS subconductance state, resulting in open probabilities of 44.6 and 42.7%, respectively. The ratio of open to closed times, however, was significantly different for the 10.8-pS subconductance state with an open probability of 57.2%.

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