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The organization of the retina of the turtle species Mauremys caspica, found in fresh water ponds of Israel, has been examined by light microscopical techniques including examination of fresh wholemount retina, one micron blue-stained vertical sections and Golgi-stained material. The anatomical findings on Mauremys retina have been compared with those of the Pseudemys retina (Kolb, 1982) which is more commonly used for electrophysiological and neurochemical studies in the USA. The photoreceptors of Mauremys are similar in type and oil droplet content to Pseudemys photoreceptors except for the double cone in Mauremys. This cone type appears more abundant than in Pseudemys and the principal member contains a yellow oil droplet instead of an orange oil droplet. Golgi staining reveals that all the cell types that have been seen in Pseudemys are found in Mauremys with identical morphology. In addition, two amacrine cell types that were not before described for Pseudemys have been added to the classification. One of these is the tristratified dopaminergic amacrine cell described in immunocytochemical studies (Witkovsky et al., 1984; Nguyen-Legros et al., 1985; Kolb et al., 1987). We have used these anatomical studies on Pseudemys and Mauremys retina to form a catalogue of neural types for the turtle retina in general. We conclude with an attempt to combine findings from anatomy, electrophysiology, and neurochemistry to form an overview of the organization of this reptilian retina.
Cone photoreceptors in the turtle retina are involved in intricate neuronal interactions with other retinal neurons that modify the responses of the cones to photons absorbed in their outer segments. Therefore, the action spectra of cones strongly depend upon the conditions of measurements. This study describes an attempt to derive the action spectra of turtle cones which are the least distorted by neuronal interactions. To achieve this goal, the photoresponses of cones and horizontal cells were recorded from the turtle retina under different conditions of adaptation using different patterns of the stimulating test flashes. The sensitivity action spectra, derived from small-amplitude (<1 mV) photoresponses, were strongly affected by the recording conditions indicating the contributions of multiple neuronal inputs. Action spectra, constructed from large criterion photoresponses, were less distorted by neuronal interactions and better described the spectral properties of the “isolated” cones. The action spectra of the hyperpolarizing inputs to chromaticity-type horizontal cells were derived by stimulating these cells with mixtures of a saturating red light and a monochromatic light of different wavelength and intensity. The action spectra were constructed from the intensity of the addend component needed to “pull down” the depolarizing response to the red component by a fixed criterion. These spectra, measured in red/green and yellow/blue C-type horizontal cells, are suggested to best represent the “isolated” M-cones and S-cones, respectively.
The effects of dopamine on luminosity-type horizontal cells have been documented in different vertebrate retinas, both in vivo and in vitro. Some of these effects may reflect direct action of dopamine onto these cells, but indirect effects mediated by presynaptic neurons cannot be ruled out. Furthermore, direct effects of dopamine on horizontal cells may affect other, postsynaptic neurons in the outer plexiform layer. To test these possibilities, we studied the effects of dopamine on photoreceptors and all types of horizontal cells in the turtle (Pseudemys scripta elegans) retina. Receptive-field properties, responsiveness to light, and time course of light responses were monitored with intracellular recordings. Dopamine at a concentration of 40 μM exerted effects with two different time courses. “Short-term” effects were fully developed after 3 min of dopamine application and reversed within 30 min of washout of the drug. “Long-term” effects were fully developed after about 7–10 min and could not be washed out during the course of our experiments. Only the “short-term” effects were studied in detail in this paper. These were expressed in a reduction of the receptive-field size of all types of horizontal cells studied; L1 and L2 luminosity types as well as Red/Green and Yellow/Blue chromaticity types. The L1 horizontal cells did not exhibit signs of reduced responsiveness to light under dopamine, while in the L2 cells and the two types of chromaticity cells responsiveness decreased. None of the rods, long-wavelength-sensitive, or medium-wavelength-sensitive cones exhibited any apparent reduction in their receptive-field sizes or responsiveness to light. The present results suggest that the “short-term” effects of dopamine are not mediated by photoreceptors and are probably due to direct action of dopamine on horizontal cells.
Long- and medium-wavelength cones in the turtle retina participate in complex neural interactions. They are coupled via excitatory pathways to other cones and receive negative feedback inputs from luminosity-type horizontal cells. Little information has been collected on the S- (short-wavelength or blue) cones because they are scarce in the turtle retina and of smaller dimensions compared to the other cone types.
In this paper, flash sensitivity action spectra and photoresponses of seven turtle S-cones were measured in the dark-adapted state and during chromatic background illuminations. The desensitizing action of monochromatic background lights was not uniform across the visible spectrum. A red background was most effective in desensitizing the S-cones to long-wavelength stimuli while a blue background light produced its strongest action on the photoresponses elicited by short-wavelength stimuli. The effects of chromatic adaptation on the S-cone action spectrum and on the kinetics of the small-amplitude photoresponses suggested that the S-cones in the turtle retina were involved in complex neural interactions. These included excitatory inputs probably originating in neighboring L-cones and inhibitory long-wavelength inputs probably mediated by L-type horizontal cells.
NADPH diaphorase histochemistry is commonly used to identify cells containing nitric oxide synthase (NOS), the enzyme catalyzing the production of nitric oxide from L-arginine. NADPH diaphorase activity and NOS immunostaining was demonstrated in different cells of the vertebrate retina; photoreceptors, horizontal cells, amacrine cells, ganglion cells, and Müller cells. However, the physiological role of nitric oxide (NO) in the retina has yet to be elucidated. In this study, we tested the assumption that NADPH diaphorase activity in the retinas of rabbits and rats depended on the state of visual adaptation. In the rabbit, light adaptation enhanced NADPH diaphorase activity in amacrine cells and practically eliminated it in horizontal cells. Dark adaptation induced the opposite effects; the NADPH diaphorase activity was reduced in amacrine cells and enhanced in horizontal cells. Retinas from eyes that were injected intravitreally with L-glutamate exhibited a pattern of NADPH diaphorase activity that was similar to that seen in dark-adapted retinas. In rats, the NADPH diaphorase activity of amacrine and horizontal cells exhibited adaptation dependency similar to that of the rabbit retina. But, the most pronounced effect of dark adaptation in the rat's retina was an enhancement of NADPH diaphorase activity in Müller cells, especially of the endfoot region. Assuming that NADPH diaphorase activity is a marker for NOS, these findings suggest that NO production in the mammalian retina is modulated by the level of ambient illumination and support the notion that NO plays a physiological role in the retina.
The role of GABA in the outer plexiform layer of the turtle retina has been examined by intracellular recordings from L- and C-type horizontal cells in the isolated retina preparation.
GABA (1–5 mM) slightly depolarized the L-type horizontal cells, reduced the amplitude of their photoresponses, and slowed down the rate of hyperpolarization during the ON component of the photoresponse. These effects could not be replicated by either muscimol or baclofen. When synaptic transmission from the photoreceptors had been blocked by either kynurenic acid or cobalt ions, GABA depolarized L-type horizontal cells and augmented the remaining photoresponses. Neither muscimol nor baclofen exerted any effect on L-type horizontal cells under these conditions. Nipecotic acid, a competitive inhibitor of the GABA-uptake system, induced effects on turtle L-type horizontal cells which were similar to those exerted by GABA. Thus, the complex GABA effect on turtle L-type horizontal cells seems to represent the summation of at least two actions; an indirect one mediated by the red cones via GABAa-type receptors and a direct one which probably reflects the activation of an electrogenic GABA-uptake system.
GABA (1–5 mM) induced a transient depolarization in C-type horizontal cells but eliminated color opponency in only three cells out of seven studied. This observation is inconsistent with the notion that the only neural mechanism responsible for the chromatic properties of C-type horizontal cells in the turtle retina is a GABAergic negative feedback from the L-type horizontal cells onto the green ones.
A technique by which the retina can be isolated from the turtle eye is described. Scanning electron microscopy revealed morphological variability between preparations and also between regions of the same one. Large areas were often totally free of any pigment epithelial cells, yet contained a high proportion of photoreceptors with complete outer segments. However, adjacent regions may contain photoreceptors without outer segments or with fragmented ones. The physiological properties of the horizontal cells also demonstrated large variability between different preparations. In all cases, lowering calcium concentration from 2 mM to 0.1−0.5 mM depolarized the horizontal cells and augmented the amplitude of the maximum photoresponses. However, these effects were accompanied by changes in the photoresponse kinetics and by a reduction in the horizontal cell sensitivity to light. Moreover, prolonged exposure to low calcium induced permanent damage to the retina as was indicated by the reduction in the response amplitude after superfusion with 2 mM calcium solution had been resumed. The toxic effects of low calcium were most apparent when superfusion with 0.1−1.0 μM calcium concentration was performed. These solutions induced complex time-dependent effects on the resting potential of horizontal cells and on the amplitude and kinetics of the photoresponses. We conclude from these observations that the normal concentration of extracellular calcium in the turtle retina is in the 2 mM range.
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
Müller cells are highly permeable to potassium
ions and play a major role in maintaining potassium homeostasis
in the vertebrate retina during light-evoked neuronal activity.
Potassium fluxes across the Müller cell's membrane
are believed to underlie the light-evoked responses of
these cells. We studied the potassium currents of turtle
Müller cells in the retinal slice and in dissociated
cell preparations and their role in the genesis of the
light-evoked responses of these cells. In either preparation,
the I–V curve, measured
under voltage-clamp conditions, consisted of inward and
outward currents. A mixture of cesium ions, TEA, and 4-AP
blocked the inward current but had no effect on the outward
current. Extracellular cesium ions alone blocked the inward
current but exerted no effect on the photoresponses. Extracellular
barium ions blocked both inward and outward currents, induced
substantial depolarization, and augmented the light-evoked
responses, especially the OFF component. Exposing isolated
Müller cells to a high potassium concentration did
not cause any current or voltage responses when barium
ions were present. In contrast, application of glutamate
in the presence of barium ions induced a small inward current
that was associated with a substantially augmented depolarizing
wave relative to that observed under control conditions.
This observation suggests a role for an electrogenic glutamate
transporter in generating the OFF component of the turtle
Müller cell photoresponse.
Horizontal cells and cone photoreceptors in the
vertebrate retina are interconnected by a complex network
of synapses leading to the generation of color-coded responses
in chromaticity horizontal cells. A simple cascade model
of excitatory feedforward and inhibitory feedback synapses
had been suggested to underlie these observations. In this
study, the photoresponses of cones and horizontal cells
were recorded intracellularly from the turtle eyecup. Three
different approaches were adopted in order to test quantitatively
the cascade model. Comparing linearity functions between
these neurons indicated multiple excitatory inputs to each
type of horizontal cells. The depolarizing photoresponses
of R/G C-type horizontal cells were considerably faster
than those of L-type horizontal cells but slower than those
recorded from L-cones. This observation disagrees with
the basic assumption of the cascade model that assign the
depolarizing photoresponses of R/G C-type horizontal cells
to a negative feedback pathway from L-type horizontal cells
onto M-cones. Finally, the action spectra of each of the
three types of horizontal cells could not be solely accounted
for by input from one spectral type of cones. Only by assuming
excitatory and inhibitory inputs from all spectral types
of cones, the action spectra of all types of horizontal
cells could be reconstructed. These findings suggest that
the negative feedback pathways from horizontal cells onto
cones in the turtle retina cannot solely account for the
chromatic properties of the horizontal cells and support
a direct inhibitory inputs from cones to turtle horizontal
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