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

2005 ◽  
Vol 22 (2) ◽  
pp. 119-133 ◽  
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.

Spontaneous regenerative activity in mammalian retinal bipolar cells: Roles of multiple subtypes of voltage-dependent Ca2+ channels

2003 ◽  
Vol 20 (2) ◽  
pp. 131-139 ◽  
Author(s):  
YU-PING MA ◽  
ZHUO-HUA PAN
Keyword(s):  
Spontaneous Activity ◽  
Bipolar Cells ◽  
Potential Oscillations ◽  
Regenerative Activity ◽  
Voltage Dependent ◽  
Cell Groups ◽  
Retinal Bipolar Cells ◽  
Ca2 Channels ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells

Patch-clamp recordings were used to investigate the properties of the regenerative activity in acutely isolated bipolar cells from the rat retina. Spontaneous, pacemaker-like membrane potential oscillations were observed in all rod bipolar cells and the majority of cone bipolar cells. The waveform of the regenerative potential was stereotypical but distinct among different bipolar cell groups, especially between rod and cone bipolar cells. The spontaneous activity was completely blocked by Co2+, suggesting that Ca2+ influx through voltage-dependent Ca2+ channels was required for initiating such activity. Ca2+-induced Ca2+ release, however, was not found to be involved. The spontaneous activity was also blocked by mibefradil, a T-type Ca2+ channel antagonist. In contrast, application of nimodipine, an L-type Ca2+ current antagonist, affected mainly the waveform of the regenerative potential. This study shows that mammalian retinal bipolar cells in isolation are also capable of generating Ca2+-dependent spontaneous regenerative potential. However, T-type Ca2+ channels appear to be essential for the initiation of the spontaneous activity in mammalian bipolar cells.

Voltage-Dependent Na+ Currents in Mammalian Retinal Cone Bipolar Cells

2000 ◽  
Vol 84 (5) ◽  
pp. 2564-2571 ◽  
Author(s):  
Zhuo-Hua Pan ◽  
Hui-Juan Hu
Keyword(s):  
Time Course ◽  
Cell Function ◽  
Signal Transmission ◽  
Bipolar Cells ◽  
Whole Cell Patch Clamp ◽  
Na Currents ◽  
Voltage Dependent ◽  
Steady State Inactivation ◽  
Retinal Bipolar Cells ◽  
Cone Bipolar Cells

Voltage-dependent Na+ channels are usually expressed in neurons that use spikes as a means of signal coding. Retinal bipolar cells are commonly thought to be nonspiking neurons, a category of neurons in the CNS that uses graded potential for signal transmission. Here we report for the first time voltage-dependent Na+ currents in acutely isolated mammalian retinal bipolar cells with whole cell patch-clamp recordings. Na+ currents were observed in ∼45% of recorded cone bipolar cells but not in rod bipolar cells. Both on and off cone bipolar cells were found to express Na+ channels. The Na+ currents were activated at membrane potentials around −50 to −40 mV and reached their peak around −20 to 0 mV. The half-maximal activation and steady-state inactivation potentials were −24.7 and −68.0 mV, respectively. The time course of recovery from inactivation could be fitted by two time constants of 6.2 and 81 ms. The amplitude of the Na+ currents ranged from a few to >300 pA with the current density in some cells close or comparable to that of retinal third neurons. In current-clamp recordings, Na+-dependent action potentials were evoked in Na+-current-bearing bipolar cells by current injections. These findings raise the possibility that voltage-dependent Na+ currents may play a role in bipolar cell function.

Mammalian Retinal Bipolar Cells Express Inwardly Rectifying K+ Currents (IKir) With a Different Distribution Than That of Ih

2003 ◽  
Vol 90 (5) ◽  
pp. 3479-3489 ◽  
Author(s):  
Yu-Ping Ma ◽  
Jinjuan Cui ◽  
Hui-Juan Hu ◽  
Zhuo-Hua Pan
Keyword(s):  
Bipolar Cells ◽  
Patch Clamp Recording ◽  
Functional Roles ◽  
Whole Cell Patch Clamp ◽  
Physiological Properties ◽  
Retinal Bipolar Cells ◽  
Inwardly Rectifying ◽  
K Currents ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells

Retinal bipolar cells comprise multiple subtypes that are well known for the diversity of their physiological properties. We investigated the properties and functional roles of the hyperpolarization-activated currents in mammalian retinal bipolar cells using whole cell patch-clamp recording techniques. We report that bipolar cells express inwardly rectifying K+ currents ( IKir) in addition to the hyperpolarization-activated cationic currents ( Ih) previously reported. Furthermore, these two currents are differentially expressed among different subtypes of bipolar cells. One group of cone bipolar cells in particular displayed mainly IKir. A second group of cone bipolar cells displayed both currents but with a much larger Ih. Rod bipolar cells, on the other hand, showed primarily Ih. Moreover, we showed that IKir and Ih differentially influence the voltage responses of bipolar cells: Ih facilitates and/or accelerates the membrane potential rebound, whereas IKir counteracts or prevents such rebound. The findings of the expression of IKir and the differential expression of Ih and IKir in bipolar cells may provide new insights into an understanding of the physiological properties of bipolar cells.

scholarly journals Differential expression of three T-type calcium channels in retinal bipolar cells in rats

2009 ◽  
Vol 26 (2) ◽  
pp. 177-187 ◽  
Author(s):  
CAIPING HU ◽  
ANDING BI ◽  
ZHUO-HUA PAN
Keyword(s):  
Visual Information ◽  
Ganglion Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Calcium Currents ◽  
Biophysical Properties ◽  
Whole Cell Patch Clamp ◽  
Voltage Dependent ◽  
Retinal Bipolar Cells ◽  
Cone Bipolar Cells

AbstractRetinal bipolar cells convey visual information from photoreceptors to retinal third-order neurons, amacrine and ganglion cells, with graded potentials through diversified cell types. To understand the possible role of voltage-dependent T-type Ca2+ currents in retinal bipolar cells, we investigated the pharmacological and biophysical properties of T-type Ca2+ currents in acutely dissociated retinal cone bipolar cells from rats using whole-cell patch-clamp recordings. We observed a broad group of cone bipolar cells with prominent T-type Ca2+ currents (T-rich) and another group with prominent L-type Ca2+ currents (L-rich). Based on the pharmacological and biophysical properties of the T-type Ca2+ currents, T-rich cone bipolar cells could be divided into three subgroups. Each subgroup appeared to express a single dominant T-type Ca2+ channel subunit. The T-type calcium currents could generate low-threshold regenerative potentials or spikes. Our results suggest that T-type Ca2+ channels may play an active and distinct signaling role in second-order neurons of the visual system, in contrast to the common signaling by L-rich bipolar cells.

Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina

1990 ◽  
Vol 63 (4) ◽  
pp. 860-876 ◽  
Author(s):  
A. Karschin ◽  
H. Wassle
Keyword(s):  
Ion Channels ◽  
Outward Current ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Similar Distribution ◽  
Isolated Cells ◽  
Membrane Hyperpolarization ◽  
Rat Retina ◽  
Inward Current ◽  
Rod Bipolar Cells

1. Bipolar cells were isolated from adult rat retinas after enzymatic and mechanical treatment. The cells could be unequivocally identified from their morphology because of high retention of their axon and dendritic processes after isolation. 2. Protein kinase C (PKC) immunoreactivity performed on sections of the rat retina labeled rod bipolar cells and a few amacrine cells. Virtually all bipolar cells in the dissociates expressed PKC immunoreactivity and were, therefore, rod bipolar cells. 3. Rod bipolar cells were examined with the tight-seal whole-cell and excised-patch recording techniques. Resting potentials of the isolated cells recorded under current-clamp conditions showed a broad unimodal distribution around -37 mV. 4. Membrane depolarization from a holding potential of -90 mV resulted in an outward current. A fast sodium inward current was not observed. Membrane hyperpolarization from a holding potential of -40 mV activated an inwardly rectifying current. 5. gamma-Aminobutyric acid (GABA) and glycine, the putative retinal neurotransmitters that mediate the bipolar cells' receptive field surround in vivo, activated chloride conductances in almost all isolated bipolar cells. GABA- and glycine-evoked currents were both desensitizing and could be antagonized by the classical blockers bicuculline, picrotoxin, and strychnine, respectively. 6. Pressure application of the drugs from fine microcapillaries to various parts of the isolated cells suggests a high GABA sensitivity at the axonal endings compared with either the somatic or dendritic region. A similar distribution was not found for glycine. On the contrary, glycine-induced single-channel events with main conductances of 52 and 34 pS were recorded from membrane patches excised from the cells' somata. 7. Conductances induced by glutamate and several excitatory amino acid agonists were observed in a number of the cells. Application of the glutamate agonist 2-amino-4-phosphonobutyric acid (APB) induced an inward current at negative holding potentials associated with the opening of ion channels. In only 5 of 93 cells, APB closed ion channels, leading to a decrease in membrane conductance.

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.

Differential expression of K+ currents in mammalian retinal bipolar cells

2002 ◽  
Vol 19 (2) ◽  
pp. 163-173 ◽  
Author(s):  
HUI-JUAN HU ◽  
ZHUO-HUA PAN
Keyword(s):  
Differential Expression ◽  
Cell Voltage ◽  
Bipolar Cells ◽  
Inactivation Kinetics ◽  
Voltage Dependent ◽  
Retinal Bipolar Cells ◽  
Kinetics Of ◽  
Retinal Cone ◽  
K Currents ◽  
Three Components

Whole-cell voltage-clamp recordings were performed to investigate voltage-dependent K+ currents in acutely isolated retinal cone bipolar cells (CBCs) from the rat. The physiological and pharmacological properties of the currents were compared with those in rod bipolar cells (RBCs). The K+ currents were found to be much larger in CBC than in RBCs. In addition, the currents in CBCs were activated and inactivated at more negative potentials. Based on the apparent inactivation property of the currents, CBCs were found to fall into two groups of cells that differed in the inactivation kinetics of IK(V) but did not correlate to the ON- and OFF-type. The IK(V) for the group of CBCs showing faster inactivation, as well as for all RBCs, contained two components with decay time constants around 0.1 and 1 s. The IK(V) for the group of CBCs showing slower inactivation only contained the slower component. Furthermore, three components of IK(V) were observed based on tetraethylammonium (TEA) sensitivity: high-sensitive, low-sensitive, and resistant component. The IK(V) for a portion of CBCs showing faster inactivation, as well as for all RBCs, contained all three components. The IK(V) for the remaining CBCs, including all of those CBCs showing slower inactivation, only contained the latter two components. This study reveals a differential expression of K+ currents in rat retinal bipolar cells, suggesting that K+ channels may play an important role in bipolar cell processing in mammalian retinas.

Unique functional properties of the APB sensitive and insensitive rod pathways signaling light decrements in mouse retinal ganglion cells

2006 ◽  
Vol 23 (1) ◽  
pp. 127-135 ◽  
Author(s):  
GUO-YONG WANG
Keyword(s):  
Functional Properties ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Mouse Retina ◽  
Clear Cut ◽  
Types Of Information ◽  
Rod Bipolar Cells ◽  
Rod Pathway ◽  
Cone Bipolar Cells

Light decrements are mediated by two distinct groups of rod pathways in the dark-adapted retina that can be differentiated on the basis of their sensitivity to the glutamate agonist DL-2-amino-phosphonobutyric (APB). By means of the APB sensitive pathway, rods transmit light decrementsviarod bipolar cells to AII amacrine cells, then to Off cone bipolar cells, which in turn innervate the dendrites of Off ganglion cells. APB hyperpolarizes rod bipolar cells, thus blocking this rod pathway. With APB insensitive pathways, rods either directly synapse onto Off cone bipolar cells, or rods pass light decrement signal to cones by gap junctions. In the present study, whole-cell patch-clamp recordings were made from ganglion cells in the dark-adapted mouse retina to investigate the functional properties of APB sensitive and insensitive rod pathways. The results revealed several clear-cut differences between the APB sensitive and APB insensitive rod pathways. The latency of Off responses to a flashing spot of light was significantly shorter for the APB insensitive pathways than those for the APB sensitive pathway. Moreover, Off responses of the APB insensitive pathways were found to be capable of following substantially higher stimulus frequencies. Nitric oxide was found to selectively block Off responses in the APB sensitive rod pathway. Collectively, these results provide evidence that the APB sensitive and insensitive rod pathways can convey different types of information signaling light decrements in the dark-adapted retina.

scholarly journals Different Contributions of GABAA and GABAC Receptors to Rod and Cone Bipolar Cells in a Rat Retinal Slice Preparation

1998 ◽  
Vol 79 (3) ◽  
pp. 1384-1395 ◽  
Author(s):  
Thomas Euler ◽  
Heinz Wässle
Keyword(s):  
Receptor Antagonist ◽  
Glutamate Receptors ◽  
Metabotropic Glutamate Receptors ◽  
Phosphinic Acid ◽  
Bipolar Cells ◽  
Resting Potential ◽  
Slice Preparation ◽  
Metabotropic Glutamate ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells

Euler, Thomas and Heinz Wässle. Different contributions ofGABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J. Neurophysiol. 79: 1384–1395, 1998. Whole cell currents were recorded from rod and cone bipolar cells in a slice preparation of the rat retina. Use of the gramicidin D perforated-patch technique prevented loss of intracellular compounds. The recorded cells were identified morphologically by injection with Lucifer yellow. During the recordings, the cells were isolated synaptically by extracellular cobalt. To distinguish the γ-aminobutyric acid (GABA) receptors pharmacologically, theGABAA receptor antagonist, bicuculline, and the GABAC receptor antagonist, 3-aminopropyl(methyl)phosphinic acid, were used. In all bipolar cells tested, application of GABA induced postsynaptic chloride currents that hyperpolarized the cells from their resting potential of about −40 mV. GABA was applied at different concentrations to allow for the different affinity of GABA at GABAA and GABAC receptors. At a GABA concentration of 25 μM, in the case of rod bipolar cells, ∼70% of the current was found to be mediated by GABAC receptors. In the case of cone bipolar cells, only ∼20% of the current was mediated by GABAC receptors. Furthermore, this GABAC-mediated fraction varied among the different morphological types of cone bipolar cells, supporting the hypothesis of distinct functional roles for the different types of cone bipolar cells. There is evidence that the efficacy of GABAC receptors is modulated by glutamate through metabotropic glutamate receptors. We tested this hypothesis by applying agonists of metabotropic glutamate receptors (mGluR)1/5 to rod bipolar cells. The specific agonist (±)-trans-azetidine-2,4-dicarboxylic acid and the potent mGluR agonist quisqualic acid reduced the amplitude of the GABAC responses by 10–30%. This suggests a functional role for the modulation of GABAC receptors by the metabotropic glutamate receptors mGluR1/5.

Distribution of protein kinase C isoforms in the cat retina

2002 ◽  
Vol 19 (5) ◽  
pp. 549-562 ◽  
Author(s):  
BOZENA FYK-KOLODZIEJ ◽  
WENHUI CAI ◽  
ROBERTA G. POURCHO
Keyword(s):  
Protein Kinase C ◽  
Protein Kinase ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Kinase C ◽  
Cat Retina ◽  
Rod Bipolar Cells ◽  
Cone Bipolar Cells

Immunocytochemical localization was carried out for five isoforms of protein kinase C (PKC) in the cat retina. In common with other mammalian species, PKCα was found in rod bipolar cells. Staining was also seen in a small population of cone bipolar cells with axon terminals ramifying near the middle of the inner plexiform layer (IPL). PKCβI was localized to rod bipolar cells, one class of cone bipolar cell, and numerous amacrine and displaced amacrine cells. Staining for PKCβII was seen in three types of cone bipolar cells as well as in amacrine and ganglion cells. Immunoreactivity for both PKCε and PKCζ was found in rod bipolar cells; PKCε was also seen in a population of cone bipolar cells and a few amacrine and ganglion cells whereas PKCζ was found in all ganglion cells. Double-label immunofluorescence studies showed that dendrites of the two PKCβII-positive OFF-cone bipolar cells exhibit immmunoreactivity for the kainate-selective glutamate receptor GluR5. The third PKCβII cone bipolar is an ON-type cell and did not stain for GluR5. The retinal distribution of these isoforms of PKC is consistent with a role in modulation of various aspects of neurotransmission including synaptic vesicle release and regulation of receptor molecules.

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