Research Article
Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells
- BRENDAN J. O'BRIEN, RANDAL C. RICHARDSON, DAVID M. BERSON
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 351-361
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Cat retinal ganglion cells of the Y (or alpha) type respond to luminance changes opposite those preferred by their receptive-field centers with a transient hyperpolarization. Here, we examine the spatial organization and synaptic basis of this light response by means of whole-cell current-clamp recordings made in vitro. The hyperpolarization was largest when stimulus spots approximated the size of the receptive-field center, and diminished substantially for larger spots. The hyperpolarization was largely abolished by bath application of strychnine, a blocker of glycinergic inhibition. Picrotoxin, an antagonist of ionotropic GABA receptors, greatly reduced the attenuation of the hyperpolarizing response for large spots. The data are consistent with a model in which (1) the hyperpolarization reflects inhibition by glycinergic amacrine cells of bipolar terminals presynaptic to the alpha cells, and perhaps direct inhibition of the alpha cell as well; and (2) the attenuation of the hyperpolarization by large spots reflects surround inhibition of the glycinergic amacrine by GABAergic amacrine cells. This circuitry may moderate nonlinearities in the alpha-cell light response and could account for some excitatory and inhibitory influences on alpha cells known to arise from outside the classical receptive field.
Temporal modulation sensitivity of tree shrew retinal ganglion cells
- HAIDONG D. LU, HEYWOOD M. PETRY
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- 18 November 2003, pp. 363-372
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Tree shrews (Tupaia belangeri) are small diurnal mammals capable of quick and agile navigation. Electroretinographic and behavioral studies have indicated that tree shrews possess very good temporal vision, but the neuronal mechanisms underlying that temporal vision are not well understood. We used single-unit extracellular recording techniques to characterize the temporal response properties of individual retinal ganglion cell axons recorded from the optic tract. A prominent characteristic of most cells was their sustained or transient nature in responding to the flashing spot. Temporal modulation sensitivity functions were obtained using a Gaussian spot that was temporally modulated at different frequencies (2–60 Hz). Sustained cells respond linearly to contrast. They showed an average peak frequency of 6.9 Hz, a high-frequency cutoff at 31.3 Hz, and low-pass filtering. Transient cells showed nonlinear response to contrast. They had a peak frequency of 19.3 Hz, a high-frequency cutoff at about 47.6 Hz, band-pass filtering, and higher overall sensitivity than sustained cells. The responses of transient cells also showed a phase advance of about 88 deg whereas the phase advance for sustained cells was about 43 deg. Comparison with behavioral temporal modulation sensitivity results suggested that transient retinal ganglion cells may underlie detection for a wide range of temporal frequencies, with sustained ganglion cells possibly mediating detection below 4 Hz. These data suggest that two well-separated temporal channels exist at the retinal ganglion cell level in the tree shrew retina, with the transient channel playing a major role in temporal vision.
Two neuropharmacological types of rabbit ON-alpha ganglion cells express GABAC receptors
- THOMAS C. ROTOLO, RAMON F. DACHEUX
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 373-384
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The major inhibitory neurotransmitters GABA and glycine provide the bulk of input to large-field ganglion cells in the retina. Whole-cell patch-clamp recordings were used to characterize the glycine- and GABA-activated currents for morphologically identified ON-α ganglion cells in the rabbit retina. Cells identified as ON-α cells by light evoked currents were intracellularly stained and examined by light microscopy which revealed dendritic stratification in the vitreal half of the inner plexiform layer and confirmed their physiological identity. All Ca2+-mediated synaptic influences were abolished with Co2+, revealing two types of ON-α cell characterized by their different inhibitory current profiles. One group exhibited larger glycine- than GABA-activated currents, while the other group had larger GABA- than glycine-activated currents. Both cell types demonstrated strychnine-sensitive glycine-activated currents and bicuculline-sensitive GABAA-activated currents. Surprisingly, both cell types expressed functional GABAC receptors demonstrated by their sensitivity to TPMPA. In addition, the cells with larger glycine-activated currents also possessed GABAB receptors, whereas those with larger GABA-activated currents did not. Immunocytochemical experiments confirmed the presence of glycine, GABAA, and GABAC receptor subunits on all physiologically identified ON-α ganglion cells in this study. In addition, the GABAB receptor immunolabeled puncta were present on the cells with larger glycine-activated currents, but not on the cells with the larger GABA-activated currents. In conclusion, the presence of different functional GABA and glycine receptors determined physiologically correlated well with the specific GABA and glycine receptor immunolabeling for two neuropharmacological types of rabbit ON-α ganglion cells.
Connexin 36 in bovine retina: Lack of phosphorylation but evidence for association with phosphorylated proteins
- ARI SITARAMAYYA, JOHN W. CRABB, DIANE F. MATESIC, ALEXANDER MARGULIS, VINITA SINGH, SADHONA PULUKURI, LOAN DANG
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 385-395
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In vertebrate retina interneuronal communication through gap junctions is involved in light adaptation and in the transfer of visual information from the rod pathway to the cone pathway. Reports over the last two decades have indicated that these gap junctions are regulated by cyclic nucleotide-dependent protein kinases suggesting that the gap junction proteins, connexins, are phosphorylated. Though all the connexins involved in light adaptation and information transfer from rod to cone pathway are not yet known, connexin 36 has been shown to be definitively involved in the latter process. We have therefore attempted to investigate the cyclic nucleotide-dependent phosphorylation of this connexin in bovine retina. We found several soluble and membrane proteins in bovine retina whose phosphorylation was regulated by cyclic nucleotides. However, no protein of about 36 kDa with cyclic nucleotide-regulated phosphorylation was found in gap junction-enriched membrane preparations. A 36-kDa phosphorylated protein was found in gap junction-enriched membranes phosphorylated in the presence of calcium. However, this protein was not immunoprecipitated by anti-connexin 36 antibodies indicating that it was not connexin 36 in spite of its similarity in molecular weight. Immunoprecipitation did reveal phosphorylated proteins coimmunoprecipitated with connexin 36. Two of these proteins were identified as beta and alpha tubulin subunits. Though cyclic GMP and calcium did not greatly influence the association of these proteins with connexin 36, the results suggest the possibility of connexin 36 associating with other proteins. Together, these observations indicate that interneuronal communication at gap junctions made by connexin 36 may not be regulated by direct phosphorylation of connexin 36, but possibly by phosphorylation of associated proteins.
Afferent connectivity to different functional zones of the optic tectum in goldfish
- M.P. PÉREZ-PÉREZ, M.A. LUQUE, L. HERRERO, P.A. NÚÑEZ-ABADES, B. TORRES
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 397-410
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This work studies the afferent connectivity to different functionally identified tectal zones in goldfish. The sources of afferents contributed to different degrees to the functionally defined zones. The dorsocentral area of the telencephalon was connected mainly with the ipsilateral anteromedial tectal zone. At diencephalic levels, neurons were found in three different regions: preoptic, thalamic, and pretectal. Preoptic structures (suprachiasmatic and preoptic nuclei) projected mainly to the anteromedial tectal zone, whereas thalamic (ventral and dorsal) and pretectal (central, superficial, and posterior commissure) nuclei projected to all divisions of the tectum. In the mesencephalon, the mesencephalic reticular formation, torus longitudinalis, torus semicircularis, and nucleus isthmi were, in the anteroposterior axis, topographically connected with the tectum. In addition, neurons in the contralateral tectum projected to the injected zones in a symmetrical point-to-point correspondence. At rhombencephalic levels, the superior reticular formation was connected to all studied tectal zones, whereas medial and inferior reticular formations were connected with medial and posterior tectal zones. The present results support a different quantitative afferent connectivity to each tectal zone, possibly based on the sensorimotor transformations that the optic tectum carries out to generate orienting responses.
The thermal contribution to photoactivation in A2 visual pigments studied by temperature effects on spectral properties
- PETRI ALA-LAURILA, RAULI-JAN ALBERT, PIA SAARINEN, ARI KOSKELAINEN, KRISTIAN DONNER
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 411-419
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Effects of temperature on the spectral properties of visual pigments were measured in the physiological range (5–28°C) in photoreceptor cells of bullfrog (Rana catesbeiana) and crucian carp (Carassius carassius). Absorbance spectra recorded by microspectrophotometry (MSP) in single cells and sensitivity spectra recorded by electroretinography (ERG) across the isolated retina were combined to yield accurate composite spectra from ca. 400 nm to 800 nm. The four photoreceptor types selected for study allowed three comparisons illuminating the properties of pigments using the dehydroretinal (A2) chromophore: (1) the two members of an A1/A2 pigment pair with the same opsin (porphyropsin vs. rhodopsin in bullfrog “red” rods); (2) two A2 pigments with similar spectra (porphyropsin rods of bullfrog and crucian carp); and (3) two A2 pigments with different spectra (rods vs. long-wavelength-sensitive (L-) cones of crucian carp). Qualitatively, the temperature effects on A2 pigments were similar to those described previously for the A1 pigment of toad “red” rods. Warming caused an increase in relative sensitivities at very long wavelengths but additionally a small shift of λmax toward shorter wavelengths. The former effect was used for estimating the minimum energy required for photoactivation (Ea) of the pigment. Bullfrog rod opsin with A2 chromophore had Ea = 44.2 ± 0.9 kcal/mol, significantly lower (one-tailed P < 0.05) than the value Ea = 46.5 ± 0.8 kcal/mol for the same opsin coupled to A1. The A2 rod pigment of crucian carp had Ea = 42.3 ± 0.6 kcal/mol, which is significantly higher (one-tailed P < 0.01) than that of the L-cones in the same retina (Ea = 38.3 ± 0.4 kcal/mol), whereas the difference compared with the bullfrog A2 rod pigment is not statistically significant (two-tailed P = 0.13). No strict connection between λmax and Ea appears to exist among A2 pigments any more than among A1 pigments. Still, the A1 → A2 chromophore substitution in bullfrog opsin causes three changes correlated as originally hypothesized by Barlow (1957): a red-shift of λmax, a decrease in Ea, and an increase in thermal noise.
The chromatic input to global motion perception
- ALEXA I. RUPPERTSBERG, SOPHIE M. WUERGER, MARCO BERTAMINI
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 421-428
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For over 30 years there has been a controversy over whether color-defined motion can be perceived by the human visual system. Some results suggest that there is no chromatic motion mechanism at all, whereas others do find evidence for a purely chromatic motion mechanism. Here we examine the chromatic input to global motion processing for a range of color directions in the photopic luminance range. We measure contrast thresholds for global motion identification and simple detection using sparse random-dot kinematograms. The results show a discrepancy between the two chromatic axes: whereas it is possible for observers to perform the global motion task for stimuli modulated along the red–green axis, we could not assess the contrast threshold required for stimuli modulated along the yellowish-violet axis. The contrast required for detection for both axes, however, are well below the contrasts required for global motion identification. We conclude that there is a significant red–green input to global motion processing providing further evidence for the involvement of the parvocellular pathway. The lack of S-cone input to global motion processing suggests that the koniocellular pathway mediates the detection but not the processing of complex motion for our parameter range.
The gap junction blockers carbenoxolone and 18β-glycyrrhetinic acid antagonize cone-driven light responses in the mouse retina
- YINGQIU XIA, SCOTT NAWY
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 429-435
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Gap junctions are widely expressed throughout the retina, and play an important role in the processing of visual information. It has been proposed that horizontal cells express unpaired gap junctions, or hemichannels, in their dendrites, and that current flowing through hemichannels reduces transmembrane voltage at cone terminals, promoting the opening of Ca2+ channels near sites of transmitter release. This model predicts that pharmacological block of gap junctions should reduce the Ca2+ current at the equivalent cone voltage, thereby decreasing the postsynaptic light response. To test this prediction, and estimate the relative magnitude of this effect on third-order cells, we recorded light responses in mouse ganglion cells under photopic conditions and applied two gap junction antagonists, carbenoxolone and the structurally related 18β-glycyrrhetinic acid (GA). Both carbenoxolone and GA decreased the size of the light response to about 30% of control. Cells that were physiologically identified as ON, OFF, or ON/OFF were equally affected by carbenoxolone/GA. These gap junction blockers did not interfere with gamma-aminobutyric acid (GABA) or glutamate receptors, as they did not affect responses to direct activation of these receptors. Under control conditions, spots larger than 200 μm in diameter activated ganglion cell receptive-field surrounds. Comparing responses to small and large spots before and during carbenoxolone treatment, we found that carbenoxolone did not preferentially inhibit surround antagonism at the ganglion cell level, but instead scaled the responses to all spot sizes. Our results extend the findings of studies in lower vertebrates which showed that light responses in horizontal cells are decreased by carbenoxolone treatment, and support the idea that hemichannels in the outer retina, most likely on horizontal cells, constitute important gates that are critical for allowing light responses to move forward into the retinal circuit. Furthermore, it suggests that ganglion cell surrounds are generated in the inner retina.
Light adaptation and color opponency of horizontal cells in the turtle retina
- GILAD TWIG, HANNA LEVY, ELITE WEINER, IDO PERLMAN
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- 18 November 2003, pp. 437-452
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Chromaticity-type (C-type) horizontal cells of the turtle retina receive antagonistic inputs from cones of different spectral types, and therefore their response to background illumination is expected to reflect light adaptation of the cones and the interactions between their antagonistic inputs. Our goal was to study the behavior of C-type horizontal cells during background illumination and to evaluate the role of wavelength in background adaptation. The photoresponses of C-type horizontal cells were recorded intracellularly in the everted eyecup preparation of the turtle Mauremys caspica during chromatic background illuminations. The voltage range of operation was either reduced or augmented, depending upon the wavelengths of the background and of the light stimuli, while the sensitivity to light was decreased by any background. The response–intensity curves were shifted to brighter intensities and became steeper as the background lights were made brighter regardless of wavelength. Comparing the effects of cone iso-luminant backgrounds on the Red/Green C-type horizontal cells indicated that background desensitization in these cells could not solely reflect background adaptation of cones but also depend upon response compression/expansion and changes in synaptic transmission. This leads to wavelength dependency of background adaptation in C-type horizontal cells, that is expressed as increased light sensitivity (smaller threshold elevation) and improved suprathreshold contrast detection when the wavelengths of the background and light stimuli were chosen to exert opponent effects on membrane potential.
Immunolocalization of TRPC channel subunits 1 and 4 in the chicken retina
- SCOTT CROUSILLAC, MICHELLE LEROUGE, MICHELE RANKIN, EVANNA GLEASON
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- Published online by Cambridge University Press:
- 18 November 2003, pp. 453-463
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In the vertebrate retina, multiple cell types express G protein-coupled receptors linked to the IP3 signaling pathway. The signaling engendered by activation of this pathway can involve activation of calcium permeable transient receptor potential (TRP) channels. To begin to understand the role of these channels in the retina, we undertake an immunocytochemical localization of two TRP channel subunits. Polyclonal antibodies raised against mammalian TRPC1 and TRPC4 are used to localize the expression of these proteins in sections of the adult chicken retina. Western blot analysis indicates that these antibodies recognize avian TRPC1 and TRPC4. TRPC1 labeling is almost completely confined to the inner plexiform layer (IPL) where it labels a subset of processes that ramify in three broad stripes. Occasionally, cell bodies are labeled. These can be found in the inner nuclear layer (INL) proximal to the IPL, the IPL, and the ganglion cell layer (GCL). Double-labeling experiments using a polyclonal antibody that recognizes brain nitric oxide synthase (bNOS) in the chicken indicate that many of the TRPC1-positive processes and cell bodies also express bNOS. Labeling with the TRPC4 antibody was much more widespread with some degree of labeling found in all layers of the retina. TRPC4 immunoreactivity was found in the photoreceptor layer, in the outer plexiform layer (OPL), in radially oriented cells in the INL, diffusely in the IPL, and in vertically oriented elements below the GCL. Double-labeling experiments with a monoclonal antibody raised against vimentin indicate that the TRPC4-positive structures in the INL and below the GCL are Müller cells. Thus, TRPC1 and TRPC4 subunits have unique expression patterns in the adult chicken retina. The distributions of these two subunits indicate that different retinal cell types express TRP channels containing different subunits.