Research Article
Noninvasive recording and response characteristics of the rat dc-electroretinogram
- NEAL S. PEACHEY, J. BRETT STANTON, ALAN D. MARMORSTEIN
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 693-701
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In response to light, the retinal pigment epithelium (RPE) generates a series of potentials that can be recorded using the dc-electroretinogram (dc-ERG). As these potentials can be related to specific cellular events, they provide information about RPE function and how that may be altered by disease or experimental manipulation. The purposes of the present study were to define a noninvasive means for recording the rat dc-ERG, to use this to define the stimulus–response properties of the major components, and to relate these results to measures of the rat electrooculogram (EOG). Parallel studies were conducted in two strains of rats (Long-Evans, LE; Sprague-Dawley, SD) that are commonly used in vision research. Rats were sedated with ketamine/xylazine and placed on a heating pad. Ag/AgCl wire electrodes were bridged with capillary tubes filled with Hanks balanced salt solution. The active electrode was placed in contact with the corneal surface and referenced to a second electrode placed within the orbit. The dc-ERG signal was amplified (dc-100 Hz), digitized, and stored offline. The duration of full-field flash stimuli was controlled using a mechanical shutter and flash luminance was controlled with neutral density filters. EOGs were recorded using subdermal platinum needle electrodes placed near the eye. In response to a 5-min light exposure, the dc-ERG of LE and SD rats included a distinct b-wave, after potential, c-wave, fast oscillation, and a slow potential of positive polarity the characteristics of which are consistent with a light peak.
Modeling receptive-field structure of koniocellular, magnocellular, and parvocellular LGN cells in the owl monkey (Aotus trivigatus)
- XIANGMIN XU, A.B. BONDS, VIVIEN A. CASAGRANDE
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 703-711
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Most cells in the retina and lateral geniculate nucleus (LGN) of primates have a concentric center/surround receptive-field organization. Details of the relationship between center and surround often can be used to predict how cells respond to visual stimuli. Models of the receptive-field organization and center/surround relationships also are useful when comparing cell classes. In the present study, we used the difference-of-Gaussians (DOG) model to quantitatively examine and compare the receptive-field center/surround organization of koniocellular (K), magnocellular (M), and parvocellular (P) LGN cells of owl monkeys. We obtained estimates of receptive-field center size (rc) and center sensitivity (Kc), and surround size (rs), and surround sensitivity (Ks) from 62 K, M, and P LGN cells by fitting their spatial-frequency responses with a DOG function (Rodieck, 1965; Croner & Kaplan, 1995). The DOG function not only accounted for the responses of P and M cells, but also provided a good description of K-cell responses. We found that at matched eccentricities of less than 15 deg, K cells had the largest rc and rs among the three cell classes. K cells also had the lowest Kc and Ks.
Calcium-induced calcium release and calcium buffering in retinal horizontal cells
- EDUARDO SOLESSIO, ERIC M. LASATER
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 713-725
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Calcium plays an integral role in intracellular signaling and process control in neurons. In the outer retina, it is a key component to the phototransduction cycle and neurotransmitter release in photoreceptor and bipolar cell terminals. It also contributes to the responses of horizontal and bipolar cells. In the dark, horizontal cells are depolarized and calcium enters via calcium permeant AMPA receptors and voltage-activated calcium channels. As a result, horizontal cells must be capable of handling high calcium loads without sustaining damage. The aim of this study was to examine the components determining the intracellular calcium levels in H2 horizontal cells in the retina of white bass. Calcium responses were evoked in isolated cells by depolarizing voltage steps and monitored by conventional imaging techniques. The responses consisted of two components: calcium entry through voltage-gated calcium channels and subsequent release from intracellular stores by calcium-induced calcium release (CICR). Under control conditions, changes in calcium levels reached 541 nM on average from a basal level of 60 nM. When release from CICR stores was blocked with ryanodine or dantrolene, calcium levels barely reached 180 nM. The threshold level needed to trigger CICR was dependent on the duration of the applied depolarization and increased in response to shorter pulses.
Spatial organization of displaced ganglion cells in the chick retina
- STEFANIA DEPLANO, NICOLETTA PEDEMONTE
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- 30 January 2003, pp. 727-734
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This study presents a morphological and quantitative analysis of displaced ganglion cells performed in the chick retina at different stages of development (E11, E17, & P2). The lipophilic dye DiI inserted into the optic nerve provided a complete staining of displaced ganglion cell population and of their dendritic trees. From 11 days of incubation (E11) all neurons present a uniform morphology and are unmistakably recognizable by the dimensions of their cell body and by the presence of the axon. Their dendritic arborizations shape a complex network through the retina. Cell bodies are randomly distributed but dendritic trees of neighboring cells constantly present two levels of dendritic overlap: about 50% of the cells present a high degree of overlap, more than the 30% up to 95% of their total area, while the other half overlaps less than 20%. The high degree of overlap identifies a cluster, which is regularly formed by three and more rarely by four neurons starting from 17 days of incubation (E17) onward and after birth. From E17 onward, 94% of clusters is constantly formed by three cells and 6% of the clusters by four neurons. The distribution and the spatial arrangement of clusters are very regular, forming a mosaic that gives rise to a precise retinal coverage. The nearest-neighbor analysis unequivocally demonstrated that the mosaic of clusters is the most regular array so far described. This exact arrangement starts from 11 days of incubation and is maintained and refined through the following stages of development and after birth.
A simple model accounts for the response of disparity-tuned V1 neurons to anticorrelated images
- JENNY C.A. READ, ANDREW J. PARKER, BRUCE G. CUMMING
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 735-753
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Disparity-tuned cells in primary visual cortex (V1) are thought to play a significant role in the processing of stereoscopic depth. The disparity-specific responses of these neurons have been previously described by an energy model based on local, feedforward interactions. This model fails to predict the response to binocularly anticorrelated stimuli, in which images presented to left and right eyes have opposite contrasts. The original energy model predicts that anticorrelation should invert the disparity tuning curve (phase difference π), with no change in the amplitude of the response. Experimentally, the amplitude tends to be reduced with anticorrelated stimuli and a spread of phase differences is observed, although phase differences near π are the most common. These experimental observations could potentially reflect a modulation of the V1 signals by feedback from higher visual areas (because anticorrelated stimuli create a weaker or nonexistent stereoscopic depth sensation). This hypothesis could explain the effects on amplitude, but the spread of phase differences is harder to understand. Here, we demonstrate that changes in both amplitude and phase can be explained by a straightforward modification of the energy model that involves only local processing. Input from each eye is passed through a monocular simple cell, incorporating a threshold, before being combined at a binocular simple cell that feeds into the energy computation. Since this local feedforward model can explain the responses of complex cells to both correlated and anticorrelated stimuli, there is no need to invoke any influence of global stereoscopic matching.
Evidence for a potential role of glucagon during eye growth regulation in chicks
- MARITA P. FELDKAEMPER, FRANK SCHAEFFEL
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 755-766
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Eye growth and refraction are regulated by visual processing in the retina. Until now, the messengers released by the retina to induce these changes are largely unknown. Previously, it was found that glucagon amacrine cells respond to defocus in the retinal image and even to its sign. The expression of the immediate-early gene product ZENK increased in this cell population in eyes wearing plus lenses and decreased in minus lens-treated chicks. Moreover, it was shown that the amount of retinal glucagon mRNA increased during treatment with positive lenses. Therefore, it seems likely that these cells contribute to the visual regulation of ocular growth and that glucagon may act as a stop signal for eye growth. The purpose of the present study was to accumulate further evidence for a role of glucagon in the visual control of eye growth. Chicks were treated with plus and minus lenses after injection of different amounts of the glucagon antagonist des-His1-Glu9-glucagon-amide or the agonist Lys17,18,Glu21-glucagon, respectively. Refractive development and eye growth were recorded by automated infrared photorefraction and A-scan ultrasound, respectively. The glucagon antagonist inhibited hyperopia development, albeit only in a narrow concentration range, and at most by 50%, but not myopia development. In contrast, the agonist inhibited myopia development in a dose-dependent fashion. At high concentrations, it also prevented hyperopia development.
A morphological classification of ganglion cells in the zebrafish retina
- WELLS I. MANGRUM, JOHN E. DOWLING, ETHAN D. COHEN
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- 30 January 2003, pp. 767-779
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We examined the distribution and morphological types of ganglion cells in the retina of the zebrafish, a model vertebrate genetic organism. Using cresyl violet and methylene blue staining, a prominent central area was observed in the ventral temporal retina. The density of ganglion cell layer neurons averaged from ∼12,000/mm2 in the dorsal-nasal retina to a peak of ∼37,000/mm2 in the ventral-temporal retina. Individual zebrafish ganglion cells were labeled by backfilling with DiI through the optic nerve followed by reconstruction using confocal microscopy. The dendritic stratification and branching pattern of each labeled ganglion cell was examined in relation to the borders of the inner plexiform layer (IPL). We identified 11 different morphological types of ganglion cell. The most commonly labeled ganglion cells were two types termed Type III or IV, which displayed highly stratified dendritic arborizations in their respective ON-, OFF-sublaminae of the IPL. Their dendritic branching patterns were highly asymmetric with many thorn-like varicosities that profusely filled the area of arborization. In contrast, Type V cells formed a small simply branching dendritic field in the innermost portion of the ON-sublamina of the IPL. Two large ganglion cell types (Types I and II) with wide monostratified dendritic fields were found in both the ON- and OFF-sublamina of the IPL. Three different types of multistratified/bistratified ganglion cells were found (Types, IX, X, and XI.) whose dendrites occupied different regions of the IPL. The multistratified dendrites of IX cells occupied the whole width of the IPL, while the dendrites of Type XI cells formed vertical claw-like endings in only the ON-sublamina of the IPL. We conclude that zebrafish ganglion cells display a rich variety of types and branching patterns. This study establishes a series of baseline measurements of zebrafish ganglion cells to facilitate examination of genes playing a role in the specification and stratification of ganglion cell types.
Temperature effects on spectral properties of red and green rods in toad retina
- PETRI ALA-LAURILA, PIA SAARINEN, RAULI ALBERT, ARI KOSKELAINEN, KRISTIAN DONNER
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 781-792
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Temperature effects on spectral properties of the two types of rod photoreceptors in toad retina, “red” and “green” rods, were studied in the range 0–38°C. Absorbance spectra of the visual pigments were recorded by single-cell microspectrophotometry (MSP) and spectral sensitivities of red rods were measured by electroretinogram (ERG) recording across the isolated retina. The red-rod visual pigment is a usual rhodopsin (λmax = 503.6 nm and 502.3 nm at room temperature (21°C) in, respectively, Bufo marinus and Bufo bufo), that of green rods (λmax = 432.6 nm in Bufo marinus) belongs to the “blue” cone pigment family. In red rods, λmax depended inversely and monotonically on temperature, shifting by −2.3 nm when temperature was raised from 0°C to 38°C. Green-rod λmax showed no measurable dependence on temperature. In red rods, warming caused a relative increase of sensitivity in the long-wavelength range. This effect can be used for estimating the energy needed for photoexcitation, giving Ea = 44.3 ± 0.6 kcal/mol for Bufo marinus rhodopsin and 48.8 ± 0.5 kcal/mol for Bufo bufo rhodopsin. The values are significantly different (P < 0.001), although the two rhodopsins have very similar absorption spectra and thermal isomerization rates. Our recording techniques did not allow measurement of the corresponding effect at long wavelengths in green rods. Although spectral effects of temperature changes in the physiological range are small and of little significance for visual function, they reveal information about the energy states and different spectral tuning mechanisms of the visual pigments.
Quantification of in vivo anaerobic metabolism in the normal cat retina through intraretinal pH measurements
- LISSA PADNICK-SILVER, ROBERT A. LINSENMEIER
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 793-806
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We examined intraretinal [H+] in the intact retina of anesthetized cats using H+-sensitive microelectrodes to obtain spatial profiles of extracellular [H+]. One H+ is produced when an anaerobically generated ATP is utilized. We theorized that H+ production directly reflects anaerobic glucose consumption. From the choroid (pH ∼7.40), [H+]o steadily increased to a maximum concentration in the proximal portion of the outer nuclear layer (pH∼7.20). The shape of the profile was always concave down, indicating that a net production of H+ occurred across the avascular outer retina. A three-layer diffusion model of the outer retina was developed and fitted to the data to quantify photoreceptor H+ extrusion into the extracellular space (QOR-H+). It was determined that the outer segment (OS) layer had negligible H+ extrusion. The data were then refitted to a special three-layer model in which the OS layer QH+ was set equal to zero, but in which the inner segments and outer nuclear layer produced H+. The resulting QOR-H+ was several orders of magnitude lower than previous measurements of QOR-lactate, which were based on choroidal mass balances of lactate.
D2-dopamine receptor blockade modulates temporal resolution in goldfish
- CARLOS MORA-FERRER, VOLKER GANGLUFF
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- Published online by Cambridge University Press:
- 30 January 2003, pp. 807-815
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A possible effect of dopamine on the temporal resolution of goldfish was investigated in a behavioral, two-alternative, forced-choice procedure. Flicker fusion frequency (FFF) was measured before and after bilateral intravitreal injections of D1- or D2-dopamine receptor (D1-/D2-R) antagonists, or after depletion of retinal dopamine by bilateral intravitreal injections of the dopaminergic neurotoxin 6-hydroxydopamine (6-OHDA). Prior to drug injections, fish achieved FFFs of 33–39 Hz. A D1-R antagonist, SCH 23390, reduced FFF by about 12% (P > 0.1), whereas a D2 antagonist, sulpiride, reduced the relative FFF by 25% (P < 0.03). Depletion of retinal dopamine with 6-OHDA induced a gradual reduction in the FFF to a maximal reduction of 50% (P < 0.001) at 2 weeks postinjection. There was recovery to control levels after 3–4 weeks postinjection. The recovery of FFF, at least in one animal, was due to the return of retinal dopamine because FFF could be reduced by intravitreal injections of sulpiride during the recovery phase. These experiments demonstrate that retinal dopamine, particularly acting on D2-R, is important for photopic temporal resolution.