Research Article
Visual processing of the zebrafish optic tectum before and after optic nerve damage
- ANGELA L. McDOWELL, LEE J. DIXON, JENNIFER D. HOUCHINS, JOSEPH BILOTTA
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 97-106
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Although the zebrafish has become an important model in visual neuroscience, little has been done to examine the processing of its higher visual centers. The purpose of this work was twofold. The first purpose was to examine the physiology of the zebrafish retinotectal system and its relationship to retinal physiology. Spectral sensitivity functions were derived from visually evoked tectal responses and these functions were compared to the functions of electroretinogram (ERG) responses obtained using the same stimulus conditions. The second purpose was to examine the recovery of visual functioning of the tectum following optic nerve damage. The optic nerves of adult zebrafish were damaged (crushed), and tectal visual processing was assessed following damage. The results showed that the spectral sensitivity functions based on the On-responses of the tectum and ERG were qualitatively similar. The functions based on each response type received similar cone contributions including both nonopponent and opponent contributions. However, the spectral sensitivity functions based on the Off-responses of the tectum and ERG differed. The results also showed that the zebrafish visual system is capable of neural regeneration. By 90 days following an optic nerve crush, the spectral sensitivity function based on the tectal On-response was similar to functions obtained from normal zebrafish. Although the tectal Off-response did recover, the spectral sensitivity based on the Off-response was not the same as the function of normal zebrafish. These results support the notion that different levels of the visual system process information differently and that the zebrafish visual system, like those of other lower vertebrates, is capable of functional regeneration.
Identification of retinal neurons in a regressive rodent eye (the naked mole-rat)
- STEPHEN L. MILLS, KENNETH C. CATANIA
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 107-117
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The retina consists of many parallel circuits designed to maximize the gathering of important information from the environment. Each of these circuits is comprised of a number of different cell types combined in modules that tile the retina. To a subterranean animal, vision is of relatively less importance. Knowledge of how circuits and their elements are altered in response to the subterranean environment is useful both in understanding processes of regressive evolution and in retinal processing itself. We examined common cell types in the retina of the naked mole-rat, Heterocephalus glaber with immunocytochemical markers and retrograde staining of ganglion cells from optic nerve injections. The stains used show that the naked mole-rat eye has retained multiple ganglion cell types, 1–2 types of horizontal cell, rod bipolar and multiple types of cone bipolar cells, and several types of common amacrine cells. However, no labeling was found with antibodies to the dopamine-synthesizing enzyme, tyrosine hydroxylase. Although most of the well-characterized mammalian cell types are present in the regressive mole-rat eye, their structural organization is considerably less regular than in more sighted mammals. We found less precision of depth of stratification in the inner plexiform layer and also less precision in their lateral coverage of the retina. The results suggest that image formation is not very important in these animals, but that circuits beyond those required for circadian entrainment remain in place.
An examination of the variables that affect express saccade generation
- PETER H. SCHILLER, JOHANNES HAUSHOFER, GEOFFERY KENDALL
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 119-127
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The frequency with which express saccades are generated under a variety of conditions in rhesus monkeys was examined. Increasing the gap time between fixation spot termination and target onset increased express saccade frequency but was progressively less effective in doing so as the number of target positions in the sample was increased. Express saccades were rarely produced when two targets were presented simultaneously and the choice of either of which was rewarded; a temporal asynchrony of only 17 ms between the targets reinstated express saccade generation. Express saccades continued to be generated when the vergence or pursuit systems was coactivated with the saccadic system.
L-type calcium channels mediate transmitter release in isolated, wide-field retinal amacrine cells
- JOZSEF VIGH, ERIC M. LASATER
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 129-134
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Transmitter release in neurons is triggered by intracellular Ca2+ increase via the opening of voltage-gated Ca2+ channels. Here we investigated the voltage-gated Ca2+ channels in wide-field amacrine cells (WFACs) isolated from the white-bass retina that are functionally coupled to transmitter release. We monitored transmitter release through the measurement of the membrane capacitance (Cm). We found that 500-ms long depolarizations of WFACs from −70 mV to 0 mV elicited about a 6% transient increase in the Cm or membrane surface area. This Cm jump could be eliminated either by intracellular perfusion with 10 mM BAPTA or by extracellular application of 4 mM cobalt. WFACs possess N-type and L-type voltage-gated Ca2+ channels. Depolarization-evoked Cm increases were unaffected by the specific N-type channel blocker ω-conotoxin GVIA, but they were markedly reduced by the L-type blocker diltiazem, suggesting a role for the L-type channel in synaptic transmission. Further supporting this notion, in WFACs the synaptic protein syntaxin always colocalized with the pore-forming subunit of the retinal specific L-type channels (CaV1.4 or α1F), but never with that of the N-type channels (CaV2.2 or α1B).
Physiological response properties of displaced amacrine cells of the adult ferret retina
- SALLY W. ABOELELA, DAVID W. ROBINSON
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 135-144
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The ganglion cell layer (GCL) of the mammalian retina contains a large number of neurons called displaced amacrine cells (DACs) that do not project to the optic nerve. However, with the exception of the rabbit starburst amacrine cell little is known regarding the function of this large population due to the difficulty experienced in making physiological recordings from these neurons. We have overcome these difficulties and have used whole-cell patch-clamp techniques to examine the intrinsic membrane properties of DACs in the ferret retina. Our results indicate a large degree of diversity in their intrinsic membrane properties. In response to maintained depolarizing current injection, DACs responded with graded depolarization or by eliciting either transient or sustained bursts of spiking activity. At the resting membrane potential, 10% of the DACs generated spontaneous spikes in either an apparently random manner or at the peak of intrinsic waves of depolarization. The resting membrane activity of the remaining DACs recorded could be classified into three groups that were quiescent (28%), had robust uncorrelated synaptic activity (30%), or underwent slow waves of depolarization (42%). Diversity was also revealed in the membrane currents recorded in voltage-clamp where some DACs were quiescent (19%), or exhibited robust nonrhythmic synaptic events (42%). The remaining DACs exhibited waves of oscillatory activity (39%), characterized by either rhythmic bursts of synaptic events (17%) or slow inward currents (22%). Bath application of 50 μM biccuculine or 150 μM picrotoxin had no effect on the waves of activity, however, the gap junction blocker, carbenoxolone (100 μm), blocked both oscillatory patterns. By including Lucifer yellow and biocytin in the recording pipette, it was possible to determine the morphology of recorded neurons and group them based on dendritic extent as small-, medium-, or large-field DACs. There were few relationships between these morphologically defined groups and their intrinsic membrane properties. The present study provides the first in-depth examination of the intrinsic membrane properties of DACs in the ferret retina and provides new insights into the potential roles these neurons play in the processing of visual information in the mammalian retina.
The type 1 polyaxonal amacrine cells of the rabbit retina: A tracer-coupling study
- LAYNE L. WRIGHT, DAVID I. VANEY
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 145-155
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The type 1 polyaxonal (PA1) cell is a distinct type of axon-bearing amacrine cell whose soma commonly occupies an interstitial position in the inner plexiform layer; the proximal branches of the sparse dendritic tree produce 1–4 axon-like processes, which form an extensive axonal arbor that is concentric with the smaller dendritic tree (Dacey, 1989; Famiglietti, 1992a,b). In this study, intracellular injections of Neurobiotin have revealed the complete dendritic and axonal morphology of the PA1 cells in the rabbit retina, as well as labeling the local array of PA1 cells through homologous tracer coupling. The dendritic-field area of the PA1 cells increased from a minimum of 0.15 mm2 (0.44-mm equivalent diameter) on the visual streak to a maximum of 0.67 mm2 (0.92-mm diameter) in the far periphery; the axonal-field area also showed a 3-fold variation across the retina, ranging from 3.1 mm2 (2.0-mm diameter) to 10.2 mm2 (3.6-mm diameter). The increase in dendritic- and axonal-field size was accompanied by a reduction in cell density, from 60 cells/mm2 in the visual streak to 20 cells/mm2 in the far periphery, so that the PA1 cells showed a 12 times overlap of their dendritic fields across the retina and a 200–300 times overlap of their axonal fields. Consequently, the axonal plexus was much denser than the dendritic plexus, with each square millimeter of retina containing ∼100 mm of dendrites and ∼1000 mm of axonal processes. The strong homologous tracer coupling revealed that ∼45% of the PA1 somata were located in the inner nuclear layer, ∼50% in the inner plexiform layer, and ∼5% in the ganglion cell layer. In addition, the Neurobiotin-injected PA1 cells sometimes showed clear heterologous tracer coupling to a regular array of small ganglion cells, which were present at half the density of the PA1 cells. The PA1 cells were also shown to contain elevated levels of γ-aminobutyric acid (GABA), like other axon-bearing amacrine cells.
Immuocytochemical analysis of spatial organization of photoreceptors and amacrine and ganglion cells in the tiger salamander retina
- JIAN ZHANG, ZHUO YANG, SAMUEL M. WU
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 157-166
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In the present study, using double- or triple-label immunocytochemistry in conjunction with confocal microscopy, we aimed to examine the population and distribution of photoreceptors, GABAergic and glycinergic amacrine cells, and ganglion cells, which are basic but important parameters for studying the structure–function relationship of the salamander retina. We found that the outer nuclear layer (ONL) contained 82,019 ± 3203 photoreceptors, of which 52% were rods and 48% were cones. The density of photoreceptors peaked at ∼8000 cells/mm2 in the ventral and dropped to ∼4000 cells/mm2 in the dorsal retina. In addition, the rod/cone ratio was less than 1 in the central retina but larger than 1 in the periphery. Moreover, in the proximal region of the inner nuclear layer (INL3), the total number of cells was 50,576 ± 8400. GABAergic and glycinergic amacrine cells made up approximately 78% of all cells in this layer, including 43% GABAergic, 32% glycinergic, and 3% GABA/glycine colocalized amacrine cells. The density of these amacrine cells was ∼6500 cells/mm2 in the ventral and ∼3200 cells/mm2 in the dorsal area. The ratio of GABAergic to glycinergic amacrine cells was larger than 1. Furthermore, in the ganglion cell layer (GCL), among a total of 36,007 ± 2010 cells, ganglion cells accounted for 65.7 ± 1.5% of the total cells, whereas displaced GABAergic and glycinergic amacrine cells comprised about 4% of the cells in this layer. The ganglion cell density was ∼1800 cells/mm2 in the ventral and ∼600 cells/mm2 in the dorsal retina. Our data demonstrate that all three major cell types are not uniformly distributed across the salamander retina. Instead, they exhibit a higher density in the ventral than in the dorsal retina and their spatial arrangement is associated with the retinal topography. These findings provide a basic anatomical reference for the electrophysiological study of this species.
Role of the cervico-ocular reflex in the “flying” pigeon: Interactions with the optokinetic reflex
- M. MAURICE, H. GIOANNI
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 167-180
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We studied the cervico-ocular reflex (COR) alone and in combination with the optokinetic (OKN) reflex in head-fixed pigeons. We analyzed these responses in two behavioral conditions: (1) animals were hung in a harness (“resting” condition); and (2) animals were additionally submitted to a frontal airflow that provoked a flight posture (“flying” condition). In both conditions, cervical stimulation provoked a slow phase of very low gain (around 0.05) in the opposite direction to that of the stimulation and fast phases triggered near the head–body alignment in the same direction as the stimulation. The slow phase showed a phase lag of 20 deg at 0.5 Hz. The gain of the slow phase was not modified by the velocity, amplitude, or frequency of the stimuli. This gain was not changed by the presence of a fixed visual surround.
When cervical stimuli (0.05–0.5 Hz) were added to an optokinetic stimulation (30 deg/s) in the “resting” condition, the slow phase velocity (SPV) of the optokinetic reflex was modulated with a time course close to that produced by the cervico-ocular reflex alone. The SPV was alternately increased and decreased round the SPV level corresponding to the steady-state OKN. In the “flying” condition, optokinetic-cervical stimulation provoked an eye beating field and a strong SPV modulation synchronized with the position of the cervical stimulation. The number of nystagmic beats (OKN) and the amplitude and velocity of the fast phases were modulated in correlation with the SPV. Consequently, the optokinetic response was increased or decreased according to whether the cervical stimuli were in the reverse direction or in the same direction as the optokinetic stimulation, respectively.
These data are interpreted as an improvement of gaze stabilization by the COR. This mechanism is context dependent, since it is strongly reinforced during the flight.
AII amacrine cells in the rabbit retina possess AMPA-, NMDA-, GABA-, and glycine-activated currents
- CHENGWEN ZHOU, RAMON F. DACHEUX
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- Published online by Cambridge University Press:
- 23 June 2004, pp. 181-188
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Physiological properties of ligand-activated currents were characterized for morphologically identified AII amacrine cells in the rabbit retina by using whole-cell recordings in a superfused retina slice preparation. The AII amacrine cells were identified based on their distinct narrow-field, bistratified morphology. In the present study, the whole-cell recordings from AII amacrine cells synaptically isolated from presynaptic influences demonstrated the presence of glutamate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid) receptors, but no kainate receptors. The presence of only AMPA receptors on rabbit AII amacrine cells is in contrast to an earlier study on rabbit AII amacrine cells by Bloomfield and Xin (2000), but consistent with previous studies on rat AII amacrine cells. In addition, NMDA (N-methyl-D-aspartate) -activated currents blocked by the NMDA antagonist D-AP7 (D-2-amino-7-phosphonoheptanoic acid) were found on the AII amacrine cells. These most likely extrasynaptic NMDA-activated currents were attenuated by the presence of Co2+ interacting with Mg2+ and Ca2+ as they competed for divalent cation-binding sites within the NMDA channel. AII amacrine cells also possessed GABA (γ-aminobutyric acid) -activated currents that were unaffected by the GABAC receptor antagonist TPMPA (1,2,5,6-tetrahydropyridine-4-yl methylphosphinic), but were completely blocked by the GABAA antagonist bicuculline. This indicates that the major inhibitory inputs were mediated by only GABAA receptors located directly on the AII amacrine cells. Furthermore, although the AII amacrine cells were glycinergic amacrine cells, they also possessed glycine-activated currents that may be mediated by autoreceptors.