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PubMedDate not supplied

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

4-Aminopyridine↗

PubMed2005

Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells.

Retinal bipolar cells are slow potential neurons that respond to photoreceptor inputs with graded potentials and do not fire action potentials. We found that transient ON bipolar cells recorded in retinal slices possess voltage-gated sodium channels located on either their dendrites or somas. The sodium currents in these neurons did not generate spikes but enhanced voltage responses evoked by visual stimulation, which selectively boosted transmission to transient ganglion cells. In contrast, sodium currents were not found in sustained ON bipolar cells, and light responses in sustained bipolar cells and ganglion cells were not affected by TTX. The presence of sodium channels in transient ON bipolar cells contributed to the separation of transient and sustained signals by selectively enhancing the responses of ON transient ganglion cells to light. Our results suggest that bipolar cell sodium channels augment transient signals and contribute to the temporal segregation of visual information.

Ambystoma↗

PubMed2003

Neurochemical heterogeneity of retinal bipolar cells.

BACKGROUND: Retinal bipolar cells show neurochemical changes in response to retinal insult, which could have profound effects on retinal function or recovery after insult however, the neurochemistry of bipolar cells is incompletely understood. METHODS The distribution of the amino acid neurotransmitters glutamate, gamma-aminobutyric acid (GABA), and glycine, and the metabolic amino acids, aspartate and glutamine, was examined immunocytochemically in the retina of the tiger salamander, a major model for the study of retinal anatomy and function. RESULTS: Each amino acid showed a unique distribution among retinal bipolar cells. All bipolar cells appear to contain glutamate and, under appropriate conditions, may also contain aspartate. GABA and glycine were restricted to a subset of conventionally placed bipolar cells located in the inner nuclear layer, but were not present in displaced bipolar cells located in the outer nuclear layer. In contrast, high levels of glutamine were almost exclusively restricted to displaced bipolar cells. Analysis of co-localization patterns revealed several different amino acid signatures within the bipolar cell population. CONCLUSIONS: The striking neurochemical heterogeneity among bipolar cells suggests important differences in signaling and metabolism that could affect cell survival, plasticity, and functional recovery from retinal insult in a cell-type-specific manner.

Ambystoma↗

PubMed1983

The spatial frequency sensitivity of bipolar cells.

Retinal bipolar cells constitute the output stage of the outer layer of the retina. There are several constraints on the ability of the bipolar cell array to respond to the different spatial frequency components of the visual image, including (i) electrical coupling in the dendritic tree receiving receptor input; (iii) the "lateral inhibition" mediated by horizontal cells. Using simple mathematical models, we derive analytical expressions for the spatial frequency response of the bipolar cell array for the case in which horizontal cells are presynaptic to bipolar cells (feedforward model) and also for the case in which horizontal cells are presynaptic to receptors (feedback model). The results illustrate the importance of the three factors mentioned in determining the bipolar cells' properties. The optimal spatial frequency for stimulating the bipolar cell array, and the range of spatial frequencies transmitted onward to the inner plexiform layer, are thus related to the anatomical and electrical properties of the cells in the outer plexiform layer.

Animals↗

PubMed1995

Pharmacology of selective and non-selective metabotropic glutamate receptor agonists at L-AP4 receptors in retinal ON bipolar cells.

Retinal ON bipolar cells possess metabotropic glutamate receptors (mGluRs) which are sensitive to L-2-amino-4-phosphonobutyric acid (L-AP4). Recent studies suggest there are multiple subtypes of L-AP4 receptors. In order to provide a more complete description of the pharmacology of the retinal L-AP4 receptor, we examined the actions of a number of compounds which are active at L-AP4 receptors and other mGluRs. Four groups of compounds were studied: (1) AP4 analogues (e.g. L-AP5, L-SOP, cyclobutylene AP5, and N-Me-AP4), (2) non-selective mGluR agonists (ibotenate and quisqualate), (3) selective mGluR agonists (L-CCG-I), and (4) agonists proposed to be selective for specific mGluR subtypes (DCG-IV and t-ADA). Concentration-response curves were obtained using the b-wave of the electroretinogram (ERG) as an assay for L-AP4 receptor activation. Whole cell voltage clamp recordings from ON bipolar cells in the retinal slice preparation of the mudpuppy were used to determine whether the compounds acted as L-AP4 receptor agonists. All compounds were L-AP4 receptor agonists, except t-ADA which was ineffective. The results reveal pharmacological differences between L-AP4 receptors in mudpuppy ON bipolar cells and those in other systems, consistent with the proposal that there are multiple L-AP4 receptor subtypes. For example, retinal L-AP4 receptors are more potently activated by L-AP5 than L-SOP, whereas L-SOP has been shown to be more potent than L-AP5 in L-AP4 receptors in the lateral perforant path (LPP) of the rat hippocampus. L-SOP is also relatively more potent at the cloned L-AP4 receptors mGluR4, 6, and 7 than in mudpuppy ON bipolar cells in situ. The different potencies of these compounds in retina and LPP is ascribed to both steric and charge factors. The results with DCG-IV and t-ADA are consistent with the proposal that these are subtype-selective agonists, but DCG-IV is likely to be selective only at very low concentrations (< or = 1 microM).

Aminobutyrates↗

PubMed2000

Activation of Ca2+--calmodulin kinase II induces desensitization by background light in dogfish retinal 'on' bipolar cells.

Retinal 'on' bipolar cells possess a metabotropic glutamate receptor (mGluR6) linked to the control of a G-protein and cGMP-activated channels which functions to generate high synaptic amplification of rod signals under dark-adapted conditions. Desensitization of 'on' bipolar cells is initiated by a rise in Ca2+ during background light too weak to adapt rod photoreceptors. Desensitization could also be elicited by raising intracellular Ca2+ above 1 microM. In order to investigate the mechanism of desensitization, whole-cell current responses to brief flashes and to steps of light were obtained from voltage-clamped 'on' bipolar cells in dark-adapted dogfish retinal slices. The inclusion of Ca2+-calmodulin kinase II (CaMKII) inhibitor peptides in the patch pipette solutions not only blocked desensitization of 'on' bipolar cells by dim background light and by 50 microM Ca2+, but also increased their flash sensitivity. The substrate of phosphorylation by CaMKII is the 'on' bipolar cell cGMP-activated channels. Desensitization probably results from a reduction in their sensitivity to cGMP and a voltage-dependent decrease in their conductance. A role for protein kinase C (PKC) in this process was excluded since activating PKC independently of Ca2+ with the phorbol ester PMA failed to induce desensitization of 'on' bipolar cells.

Animals↗

PubMed1990

Time-dependent reduction of glutamate current in retinal bipolar cells.

Glutamate hyperpolarizes retinal depolarizing bipolar cells (DBCs) by decreasing a non-specific cation conductance. We have investigated this action of glutamate using whole-cell voltage clamp of DBCs in larval tiger salamander retinal slices and here report two observations: a wash-out of the glutamate response and a concomitant decrease in resting membrane conductance. The wash-out may be due to the loss of a second messenger-mediated mechanism linking the receptor to the response. The decrease in resting membrane conductance suggests that this second messenger may be required to maintain DBC glutamate channels in an open state in the absence of the receptor ligand.

Animals↗

PubMed1988

Membrane currents of retinal bipolar cells in culture.

1. Retinal bipolar cells were isolated from white bass retinas and maintained in a cell culture preparation. Two morphological types of bipolar cells were observed in cell culture. These were labeled large- and small-bipolar cells based mainly on the size of their somata and primary dendrites. Two types of small-bipolar cells were observed. Isolated bass bipolar cells are very similar to those described in the intact retina. 2. Under current clamp, to depolarizing current injection, small-bipolar cells produced a spike followed by a plateau. Large-bipolar cells showed a slow depolarization to a plateau level. 3. Voltage-gated membrane currents were studied using whole-cell patch-clamp techniques. Channel blocking agents were used to define the ion channels found in the membranes of these cells. 4. The large-bipolar cells were found to possess an A-current, a calcium current, and a calcium-dependent potassium current. 5. Large bipolar cells also possessed an inward rectifier that did not correspond to any previously described. 6. The two types of small-bipolar cells were found to have very similar membrane properties to one another. They lacked a large A-current but possessed a slowly activating, outward rectifying potassium current. Similar to the large-bipolar cells, they showed a calcium current and a calcium-activated potassium current. 7. The inward rectifier of small-bipolar cells was characterized as an H-current. 8. The results suggest that the membrane currents of bipolar cells set a narrow operating range about which the cells function in the intact retina. In addition these currents help shape the responses of bipolar cells to light stimuli but do not confer ON or OFF properties.

Animals↗

PubMed2003

Uncoupling of horizontal cells alters the receptive fields of retinal bipolar cells.

Effects of uncoupling of horizontal cells by 1-octanol, a non-specific gap junction uncoupling agent, on the receptive field organization of cone-dominant bipolar cells were investigated in isolated, superfused carp retina, using intracellular recording techniques. At 1 mM, 1-octanol increased responses of cone driven horizontal cells to light spots, but decreased those to light annuli, indicating a reduction of the receptive field size of these cells by uncoupling. Furthermore, 1-octanol eliminated the surround response of OFF type bipolar cells and increased their center response. Similar effects of 1-octanol on the center and surround responses were observed in ON type bipolar cells. These results suggest that uncoupling of horizontal cells can significantly alter the receptive field organization of retinal bipolar cells.

1-Octanol↗

PubMedDate not supplied

Relation between potassium-channel kinetics and the intrinsic dynamics in isolated retinal bipolar cells.

Characterization of the intrinsic dynamics of isolated retinal bipolar cells by a whole-cell patch-clamp technique combined with estimation of effective impulse responses across a range of mean injected currents reveals strikingly adaptive behavior. At resting potential, bipolar cells' effective impulse response is slow, high gain, and low pass. Depolarization speeds up response, decreases gain, and, in most cells, induces bandpass behavior. This adaptive behavior involves two K(+) currents. The delayed-rectifier accounts for the observed gain reduction, speed increase, and bandpass behavior. The A-channel further shortens the impulse responses but suppresses bandpass features. Computer simulations of model neurons with a delayed-rectifier and varying A-channel conductances reveal that impulse responses largely reflect the flux of electrical charge through the two K(+) channels. The A-channel broadens the frequency response and preempts the action of the delayed-rectifier, thereby reducing the associated bandpass features. Admixtures of the two K(+) channels produce the observed variety of dynamics of retinal bipolar cells.

4-Aminopyridine↗

PubMedDate not supplied

Voltage-activated Ca2+ channels and ionotropic GABA receptors localized at axon terminals of mammalian retinal bipolar cells.

A preparation of isolated presynaptic terminals of rat retinal rod bipolar cells was developed. Patch-clamp recordings were performed on the isolated terminal to determine the type(s) of voltage-activated Ca2+ channels and the contribution of GABA(A) and GABA(C) receptor-mediated currents localized in the terminal region. Both low-voltage-activated (LVA) and high-voltage-activated (HVA) Ca2+ currents, with properties similar to those found in intact cell recordings, were observed in the isolated terminal recordings. Consistent with previous studies, the HVA Ca2+ currents are L-type since the currents were blocked by low micromolar concentrations of nimodipine and potentiated by BayK 8644. Also, both GABA(A) and GABA(C) receptor-mediated currents were observed in the isolated terminal. The current density of GABA(C) receptors in the terminal was more than three times higher than that in the soma. In contrast, the current density of GABA(A) currents between the terminal and the soma was not significantly different. Assessed by 100 microM GABA, the contributions of GABA(A) and GABA(C) receptors to the total GABA-mediated currents at the terminal were comparable. This study directly demonstrates the localization of LVA Ca2+ channels at the axon terminal of mammalian rod bipolar cells, suggesting that LVA Ca2+ channels may play a role in bipolar cell transmitter release. Results of this study also support the notion that both types of ionotropic GABA receptors regulate synaptic transmission in mammalian rod bipolar cells. In addition, this study reports for the first time the feasibility of direct patch-clamp recordings of isolated axon terminals of mammalian retinal bipolar cells. The isolated presynaptic terminal preparation of mammalian retinal bipolar cells could be a valuable system for the study of transmitter release in the central nervous system (CNS).

3-Pyridinecarboxylic acid, 1,4-dihydro-2,6-dimethy↗

PubMed2000

Subcellular localization and complements of GABA(A) and GABA(C) receptors on bullfrog retinal bipolar cells.

gamma-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 GABA(A) and GABA(C) receptors 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 GABA(A) receptor antagonist, and imidazole-4-acetic acid (I4AA), a GABA(C) 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 GABA(A) and GABA(C) receptors. Subcellular localization and complements of GABA(A) and GABA(C) receptors at the dendrites and axon terminals were highly related to the dichotomy of OFF and ON BCs. In the case of OFF BCs, GABA(A) receptors were rather evenly distributed at the dendrites and axon terminals, but GABA(C) receptors were predominantly expressed at the axon terminals. Moreover, the relative contribution of GABA(C) receptors to the axon terminals was prevalent over that of GABA(A) receptors, while the situation was reversed at the dendrites. In the case of ON BCs, GABA(A) and GABA(C) 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 GABA(C) receptors were much less expressed than GABA(A) receptors. GABA(A), but not GABA(C) receptors, were expressed clusteringly at axons of a population of BCs. In a minority of BCs, I4AA suppressed the GABA(C) responses at the dendrites, but not at the axon terminal, implying that the GABA(C) receptors at these two sites may be heterogeneous. Taken together, these results suggest that GABA(A) and GABA(C) 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.

6-Cyano-7-nitroquinoxaline-2,3-dione↗

PubMed2004

Evidence that certain retinal bipolar cells use both glutamate and GABA.

Retinal bipolar neurons release the excitatory transmitter, glutamate. However, certain bipolar cells contain GABA, raising the question whether a neuron might release both transmitters and, if so, what function might the inhibitory transmitter play in a particular circuit? Here we identify a subset of cone bipolar cells in cat retina that contain glutamate, plus its vesicular transporter (VGLUT1), and GABA, plus its synthetic enzyme (GAD(65)) and its vesicular transporter (VGAT). These cells are negative for a marker of ON bipolar cells and restrict their axons to the OFF strata of the inner synaptic layer. They do not colocalize with the neurokinin 3 receptor that stains a type (or two) of OFF bipolar cells. By "targeted injection," we identified two types of OFF bipolar cell with the machinery to make and package both transmitters. One of these types costratifies with a dopamine plexus.

Animals↗

PubMed2004

Retinal bipolar cell input mechanisms in giant danio. II. Patch-clamp analysis of on bipolar cells.

Glutamate receptors on giant danio retinal on bipolar cells were studied with whole cell patch clamping using a slice preparation. Cone-driven on bipolars (Cbs) and mixed-input on bipolars (Mbs) were identified morphologically. Most Cbs responded to the excitatory amino acid transporter (EAAT) substrate d-aspartate but not to the group III metabotropic glutamate receptor (mGluR) agonist l-(+)-2-amino-4-phosphonobutyric acid (l-AP4) or the AMPA/kainate receptor agonist kainate, suggesting EAATs are the primary glutamate receptors on Cbs. The EAAT inhibitor dl-threo-beta-benzyloxyasparate (TBOA) blocked all light-evoked responses of Cbs, suggesting these responses are mediated exclusively by EAATs. Conversely, all Mbs responded to d-aspartate and l-AP4 but not to kainate, indicating they have both EAATs and group III mGluRs (presumably mGluR6). The light responses of Mbs involve both receptors because they could be blocked by TBOA plus (RS)-alpha-cyclopropyl-4-phosphonophenylglycine (CPPG, a group III mGluR antagonist) but not by either alone. Under dark-adapted conditions, the responses of Mbs to green (rod-selective) stimuli were reduced by CPPG but enhanced by TBOA. In contrast, both antagonists reduced the responses to red (cone-selective) stimuli, although TBOA was more effective. Furthermore, under photopic conditions, TBOA failed to eliminate light-evoked responses of Mbs. Thus on Mbs, rod inputs are mediated predominantly by mGluR6, whereas cone inputs are mediated mainly by EAATs but also by mGluR6 to some extent. Finally, we explored the interactions between EAATs and mGluR6 in Mbs. Responses to d-aspartate were reduced by l-AP4 and vice versa. Therefore mGluR6 and EAATs suppress each other, and this might underlie mutual suppression between rod and cone signals in Mbs.

Aminobutyrates↗

PubMed1999

The metabotropic receptor mGluR6 may signal through G(o), but not phosphodiesterase, in retinal bipolar cells.

Bipolar cells are retinal interneurons that receive synaptic input from photoreceptors. Glutamate, the photoreceptor transmitter, hyperpolarizes On bipolar cells by closing nonselective cation channels, an effect mediated by the metabotropic receptor mGluR6. Previous studies of mGluR6 transduction have suggested that the receptor couples to a phosphodiesterase (PDE) that preferentially hydrolyzes cGMP, and that cGMP directly gates the nonselective cation channel. This hypothesis was tested by dialyzing On bipolar cells with nonhydrolyzable analogs of cGMP. Whole-cell recordings were obtained from On bipolar cells in slices of larval tiger salamander retina. Surprisingly, On bipolar cells dialyzed with 8-(4-chlorophenylthio)-cyclic GMP (8-pCPT-cGMP), or 8-bromo-cyclic GMP (8-Br-cGMP) responded normally to glutamate or L-2-amino-4-phosphonobutyrate (L-APB). Response amplitudes and kinetics were not significantly altered compared with cells dialyzed with cGMP alone. Comparable results were obtained with the PDE inhibitor 3-isobutyl-1-methyl-xanthine (IBMX) or with 8-pCPT-cGMP and IBMX together, indicating that PDE is not required for mGluR6 signal transduction. Addition of the G-protein subunit G(o)alpha to the pipette solution suppressed the cation current and occluded the glutamate response, whereas dialysis with G(i)alpha or with transducin Gbetagamma had no significant effect on either the cation current or the response. Dialysis of an antibody directed against G(o)alpha also reduced the glutamate response, indicating a functional role for endogenous G(o)alpha. These results indicate that mGluR6 may signal through G(o), rather than a transducin-like G-protein.

1-Methyl-3-isobutylxanthine↗

PubMed2003

Mammalian retinal bipolar cells express inwardly rectifying K+ currents (IKir) with a different distribution than that of Ih.

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.

Action Potentials↗

PubMed2004

Stratum-by-stratum projection of light response attributes by retinal bipolar cells of Ambystoma.

The visual system processes light images by projecting various representations of the visual world to segregated regions in the brain through parallel channels. Retinal bipolar cells constitute the first parallel channels that carry different light response attributes to different parts of the inner plexiform layer (IPL). Here we present a systematic study on detailed axonal morphology and light response characteristics of over 200 bipolar cells in dark-adapted salamander retinal slices by the whole-cell voltage clamp and Lucifer yellow fluorescence (with a confocal microscope) techniques. Four major groups of bipolar cells were identified according to the patterns of axon terminal ramification in the IPL: 36% were narrowly monostratified (whose axon terminals ramified in one of the 10 strata of the IPL), 27% were broadly monostratified, 19% were multistratified, and 18% bore pyramidally branching axons. By analysing the bipolar cells with narrowly monostratified axon terminals in each of the 10 strata of the IPL, we found that several key light response attributes are highly correlated with the strata in which the cells' axon terminals ramify. The 10 IPL strata appear to be the basic building blocks for attributes of light-evoked signal outputs in all bipolar cells, and several general stratum-by-stratum rules were identified by analysing the broadly monostratified, multistratified and pyramidally branching cells. These rules not only uncover mechanisms by which third-order retinal cells integrate and compute bipolar cell signals, but also shed considerable light on how bipolar cells in other vertebrates process visual information and how physiological signals may shape the morphology and projection of output synapses of visual neurones during development.

Adaptation, Ocular↗

PubMed1999

Zn2+ differentially modulates kinetics of GABA(C) vs GABA(A) receptors in carp retinal bipolar cells.

GABA(C) and GABA(A) receptors co-exist in retinal bipolar cells. In the present study the effects of zinc on the kinetics of currents mediated by GABA(C) and GABA(A) receptors were investigated in isolated carp bipolar cells, using whole-cell patch-clamp technique. We observed for the first time that zinc exerted opposite effects on kinetics of the GABA(C) and GABA(A) responses: zinc significantly slowed down activation and desensitization of the GABA(C) response, but accelerated those of the GABA(A) response; zinc dramatically accelerated deactivation of the GABA(C) response, whereas it had no apparent effect on deactivation of the GABA(A) response. These results suggest that zinc may be functionally important in regulating retinal signal transmission.

Animals↗