Effects of electrical coupling on the cone-horizontal cell circuit in the catfish retina

Based on experimental data, a model of the cone-horizontal cell (L-HC) circuit has been developed for the luminosity channel of the catfish retina and impulse responses of cones and L-HC's were replicated for various experimental conditions. Negative feedback from L-HC to the cone pedicle and increases in the dc levels of L-HC (H ⁰), that produce increases in the feedback gain, convert monophasic impulse responses to those that are biphasic, smaller and faster. Electrical coupling of cones and L-HC's lead to decremental spread of 2 radially outgoing waves with time courses of the coupled cones and L-HC's dependent on the spatial organization of the negative feedback circuit: however, the L-HC's impulse response on spreading outward shows an initial increase before decreasing. Interactions of the cone and L-HC waves were studied using Laplace transforms and the convolution theorem. The presence of a negative feedback circuit leads to deviations of the electrotonic decay from an exponential function. As a result of the dependency of the feedback gain on H ⁰, electrical coupling introduces non-linearities in the cone-L-HC circuit that are dependent on the mean illuminance level.     

Modelling the effects of a negative feedback circuit from horizontal cells to cones on the impulse responses of cones and horizontal cells in the catfish retina

A model of the cone-L-HC circuit for the catfish retina is presented with the following features: the outer segment consists of a compression factor and 7 low-pass filters in tandem; the cone pedicle consists of an internal negative feedback circuit in series with a low-pass filter; and the L-HC consists of a low-pass filter and forms a negative feedback circuit with the cone pedicle. By proper adjustment of the various time constants of the low-pass filters and the gain factors, the impulse responses for cones and L-HCs of the catfish retina (and turtle) can be duplicated. The negative feedback gain increases with increasing levels of mean illuminance which causes the monophasic impulse responses to become faster, biphasic and decrease in amplitude, i.e. in gain. This is an expression of the Weber-Fechner law.     

Model of the cone-horizontal cell circuit in the catfish retina

A model of the cone-L-type horizontal cell circuit of the catfish contains 3 stages. The outer segment consists of a compression factor producing the Naka-Rushton relationship between amplitude of response and intensity and 7 low-pass filters in tandem that produces an absolute delay of about 15 ms. The cone pedicle consists of an internal negative feedback circuit in series with a low-pass filter. The L-type horizontal cell acts as a linear low-pass filter and forms the external negative feedback circuit with the cone pedicle. The system shows peicewise linearity with the feedback gain of the external negative feedback circuit directly proportional to the dc level of the horizontal cell. Thus, at any given mean illuminance the impulse response of the cone and L-HC adequately defines the dynamics of the responses. The conversion of a slow monophasic to a faster biphasic impulse response due to either an increase in mean illuminace or use of a steady annulus results from the change in the characteristic equation as the effective value of the feedback gain changes. By proper adjustement of gains and time constants, the cone-L-HC circuit of the catfish retina simulates the experimental data.     

Dynamics of chromatic adaptation in cones of freshwater turtle

The closer the wavelength of a steady background of monochromatic light is to the peak sensitivity of a cone that is being illuminated, the stronger is the desensitization of that cone; this is chromatic adaptation. A model of the freshwater turtle retina with the neural components of chromatic adaptation via negative feedback circuits is used to simulate and study various aspects of chromatic adaptation. An internal negative feedback circuit resides solely within the cone pedicle and thereby, its adaptive effects are relatively specific, so that univariance is maintained. The cone-L-horizontal cell circuit is an external negative feedback circuit and its adaptive effects are less specific since all 3 chromatic cone types are involved, so that univariance is violated. Chromatic adaptation is the result of the decrease in the cone gain due to the dependency of the gains of the negative feedback circuits on the mean illuminance level. The results of the model are consistent with von Kries law, but the changes in gains of the cones due to chromatic adaptation are dependent on wavelength, intensity of the adapting light and size.     

Dynamics of chromaticity horizontal cells in the freshwater turtle retina

A model of the cone-horizontal cell circuit is presented based on morphological evidence recently found in the Reeves' turtle: a luminosity horizontal cell (LHC) that receives inputs from red-, green-, and blue-sensitive cones in the ratio of 15:3:1, a triphasic horizontal cell (THC) that receives inputs from one class of red-sensitive and from blue-sensitive cones in the ratio of 2:1; and a biphasic chromaticity horizontal cell (BHC) that receives inputs from green-sensitive cones as well as from a special class of red-sensitive (i.e. the broad spectrum) and from blue-sensitive cones in the ratio of 3:2:1. A study of the simulated impulse responses strongly suggests that the basic response patterns of the BHC and THC can be readily explained by a simple wiring diagram consisting of direct hyper-polarizing inputs from the appropriate cones and a depolarizing input from the LHC which acts as a voltage inverter. A negative feedback circuit from the LHC to the cone pedicles is included and its negative feedback gain increases as the mean illuminance level (Io) increases. The negative feedback circuit, which promotes adaptation in the cones to changing Io's, is not necessary for opponent polarization in the BHC or THC, but does explain variabilities of impulse responses.     

Modeling of the vertebrate visual system. II. Application to the turtle cone retina

The model of the vertebrate cone retina was adapted to the turtle retina with its red cone- and L-channel-dominances. The model consists of an ordering of four spatial organizations of unit hexagons, weighted inputs for all cones in the receptive fields, and linear polarization factors based on data from literature on turtle retina. Data generated by the model for spatial and chromatic patterns of receptive fields, intensity-response curves, dynamic ranges for cones, horizontal and bipolar cells proved remarkably consistent with literature. The model also generates observed phenomena such as near-field enhancement of cones due to stray light effects and electrical coupling of like-cones and far-field decrease in responses due to negative feedback from L-type horizontal cells to cones. Annular stimuli were shown to be more effective than spot stimuli for horizontal cells. The formal approach of the model demonstrates factors which play roles in various observed phenomena and all aspects of model can be displayed and tested both qualitatively and quantitatively.     

Feedback connections and operation of the outer plexiform layer of the retina.

The primary feedback control apparatus in the outer retina is the sign-inverting feedback synapse between horizontal cells and cones. In many lower vertebrates horizontal cells release GABA in darkness, which opens Cl- channels in cones. Input-output relations of the feedback synapse reveal that the synaptic gain is light-dependent with the highest negative gain near the dark horizontal cell potential. The horizontal cell-cone feedback synapse improves the reliability of the photoreceptor output synapses. It also modulates the dynamic range and mediates color opponency and surround responses in second-order retinal neurons.     

Dynamics of L-type bipolar and phasic amacrine cells in the vertebrate cone retina

The model of the cone-L-HC circuit of the catfish retina (Siminoff 1985a) is extended to Luminosity bipolar cells (BC) and non-linear phasic amacrine cells (AC), but now applicable to the generalized vertebrate cone retina that involves only one cone type. Two types of BC's are simulated by linear transformation of 2 antagonistic inputs of differing time courses; the faster center field hyperpolarization from the cone and the slower surround field depolarization from the L-HC. The phasic AC was made non-linear by various methods: full- or half-wave rectification using either both or only one of the BC's as the inputs with rectification first and then summation or summation first and then rectification. A method is described using Laplace transforms in conjunction with the convolution theorem to obtain the impulse responses of BC's and AC's, in spite of the non-linearities of the AC even when used as feedback to the BC's. Since the input to the BC consists of 2 antagonistic inputs, feedback from the AC reeinforces one input and attenuates the other.     

Photoresponse ontogeny and its relation to development of pineal organ and eye in larval bagrid catfish Mystus nemurus (Valenciennes)

The artificially reared bagrid catfish Mystus nemurus was observed for the histological development of the pineal organ and retina and photoresponse in a test tank at hatching to 14?d after hatching. The pineal organ was functional at hatching, and the lens-like tissue was partly ossified forming a pineal window at 6?d. The retina became morphologically functional when the outer segments of single cones were formed, and the eyes were innervated with the optic tectum at 18?h and rods were formed at 36?h. Long and thin single cones were not observed. The larvae exhibited undirected kinetic movement at hatching to 12?h and directed tactic swimming away from a torch after 18?h in response to a torch light. The photoresponse of the larvae was negative at hatching to 30?h and at 6?d to the end of the observation at 14?d, but neutral during a period at 36?h to 5?d. It was evident that the kinetic movement was mediated by light perception with the pineal organ, which was not capable of detecting directed signal information, and that the larvae were capable of directed tactic movement only when vision was involved. The vigorous negative phototaxis at 6–14?d was attributed to the improvement of photosensitivity of the retina and the pineal organ.     

Cones in the retina of the catfish, Clarias batrachus (L.)

The retina of the catfish Clarias butrachus (L.), supposed to possess an all-rod retina, is found on re-investigation to contain both rods and cones. The retina is characterized by a prominent tapetum and multiple optic papillae.     

Landolt's club in the retina of catfish, Heteropneustes fossilis: a new finding in Teleostei

The visual cells in the retina of the freshwater catfish, Heteropneustes fossilis comprise rods, long single cones, short single cones and Landolt's clubs.     

Intrinsic cone adaptation modulates feedback efficiency from horizontal cells to cones.

Processing of visual stimuli by the retina changes strongly during light/dark adaptation. These changes are due to both local photoreceptor-based processes and to changes in the retinal network. The feedback pathway from horizontal cells to cones is known to be one of the pathways that is modulated strongly during adaptation. Although this phenomenon is well described, the mechanism for this change is poorly characterized. The aim of this paper is to describe the mechanism for the increase in efficiency of the feedback synapse from horizontal cells to cones. We show that a train of flashes can increase the feedback response from the horizontal cells, as measured in the cones, up to threefold. This process has a time constant of approximately 3 s and can be attributed to processes intrinsic to the cones. It does not require dopamine, is not the result of changes in the kinetics of the cone light response and is not due to changes in horizontal cells themselves. During a flash train, cones adapt to the mean light intensity, resulting in a slight (4 mV) depolarization of the cones. The time constant of this depolarization is approximately 3 s. We will show that at this depolarized membrane potential, a light-induced change of the cone membrane potential induces a larger change in the calcium current than in the unadapted condition. Furthermore, we will show that negative feedback from horizontal cells to cones can modulate the calcium current more efficiently at this depolarized cone membrane potential. The change in horizontal cell response properties during the train of flashes can be fully attributed to these changes in the synaptic efficiency. Since feedback has major consequences for the dynamic, spatial, and spectral processing, the described mechanism might be very important to optimize the retina for ambient light conditions.     

Evaluation of Turtle Exclusion and Escapement Devices for Hoop-Nets

Abstract Baited and unbaited hoop-nets commonly are used to capture catfish in lotic and lentic systems. Turtle bycatch and post-capture mortality has been problematic during catfish surveys in Missouri, USA, most recently in the Gasconade River, Gasconade and Osage counties. We evaluated 3 modified hoop-net designs that would reduce turtle bycatch without reducing catfish capture in the Gasconade River during 15 May-15 July 2006 after pilot study evaluation of 5 hoop-net designs in April 2006. We deployed modified and control-nets in blocks for 48 hours to evaluate differences in turtle and catfish catch rate, as well as abundance, size, and mortality rate of turtle bycatch. The chimney design reduced turtle bycatch by 84% when compared to the control, without decreasing the number or average size of captured flathead catfish (Pylodictis olivaris). Environmental conditions that affected turtle mortality included Secchi disc transparency, temperature, dissolved oxygen, and stream river depth. This is the first known attempt to create turtle exclusion or escapement devices for hoop-nets deployed in freshwater systems. Biologists using hoop-nets to sample aquatic vertebrates in moderate to large river systems will benefit from our study. The application of this methodology will reduce turtle bycatch mortality, especially when sampling is conducted in high water temperatures.     

Photoreceptors and cone patterns in the retina of the smelt Osmerus eperlanus (L.) (Osmeridae: Teleostei)

The outer retina of the smelt Osmerus eperlanus, a visually orientated plankton feeder, of Lake Hiidenvesi (Finland), was examined using both light and transmission electron microscopy. Apart from rods, six morphologically different cone photoreceptor types were identified: short single cones, long single cones, unequal/equal double cones and triple cones (triangular and linear variety). Additionally, in the dorsal region, multiple cone arrangements consisting of up to five members occur. Long single cones and triple cones were observed only sporadically throughout the retina. The incidence of short single cones as a regular element of the cone mosaic is restricted to the ventrotemporal area. The dominant pattern in the Osmerus retina is a pure or a twisted row pattern occurring in all regions. Ventrotemporally, however, square patterns were found as well. The highest cone densities occur in the peripheral ventrotemporal retina. These results indicate that the ventrotemporal region plays an important role in the vision of the smelt. The findings are discussed with respect to the photic habitat conditions and behavioural ecology of the smelt in Lake Hiidenvesi.     

Spatial and temporal properties of luminosity horizontal cells in the turtle retina

Luminosity horizontal cells in the turtle retina respond approximately linearly to visual stimuli with contrast levels spanning a large part of the physiological range. We characterized the response properties of these cells under conditions of low photopic background illumination by measuring their spatial and temporal frequency transfer functions. Our experimental results indicate in two ways that, under these conditions, feedback from luminosity horizontal cells to cones does not play a major role in the mechanisms underlying the spatial and temporal tuning of horizontal cell responses. First, the shape of the spatial transfer function depended only weakly on the temporal frequency with which it was measured. Second, the shape of the temporal transfer function depended only weakly on the spatial frequency with which it was measured.     

Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels

In the vertebrate retina, horizontal cells generate the inhibitory surround of bipolar cells, an essential step in contrast enhancement. For the last decades, the mechanism involved in this inhibitory synaptic pathway has been a major controversy in retinal research. One hypothesis suggests that connexin hemichannels mediate this negative feedback signal; another suggests that feedback is mediated by protons. Mutant zebrafish were generated that lack connexin 55.5 hemichannels in horizontal cells. Whole cell voltage clamp recordings were made from isolated horizontal cells and cones in flat mount retinas. Light-induced feedback from horizontal cells to cones was reduced in mutants. A reduction of feedback was also found when horizontal cells were pharmacologically hyperpolarized but was absent when they were pharmacologically depolarized. Hemichannel currents in isolated horizontal cells showed a similar behavior. The hyperpolarization-induced hemichannel current was strongly reduced in the mutants while the depolarization-induced hemichannel current was not. Intracellular recordings were made from horizontal cells. Consistent with impaired feedback in the mutant, spectral opponent responses in horizontal cells were diminished in these animals. A behavioral assay revealed a lower contrast-sensitivity, illustrating the role of the horizontal cell to cone feedback pathway in contrast enhancement. Model simulations showed that the observed modifications of feedback can be accounted for by an ephaptic mechanism. A model for feedback, in which the number of connexin hemichannels is reduced to about 40%, fully predicts the specific asymmetric modification of feedback. To our knowledge, this is the first successful genetic interference in the feedback pathway from horizontal cells to cones. It provides direct evidence for an unconventional role of connexin hemichannels in the inhibitory synapse between horizontal cells and cones. This is an important step in resolving a long-standing debate about the unusual form of (ephaptic) synaptic transmission between horizontal cells and cones in the vertebrate retina.     

Ontogeny of Double Cones in the Retina of Perch Fry (Perca fluviatilis,Teleostei)

The formation of double cones in the retina of fry of Perca fluviatilis has been investigated by light and electron microscopy. The retina of newly hatched fry is provided with single cones and rods, single cones being the predominant receptor type. Double cones are seen for the first time 22 days after hatching. Mitoses are observed in the periphery of the retina, but are also seen in more central parts of the retina containing differentiated receptors and a cone mosaic. The fate of the cells resulting from the centrally located mitoses is not known. No signs of longitudinal fission of differentiated single cones are seen. It is suggested that double cones in the retina of perch fry arise by fusion of single cones which associate closely and develop subsurface cisterns coextensive with the region of intimate contact in the ellipsoid. During the first few weeks after hatching, there is a gradual shift in arrangement of the cones. In the newly hatched fry, the single cones are arranged in rows. When double cones are first seen, square-pattern units appear, built up from four double cones and a single cone.     

Dim light vision – Morphological and functional adaptations of the eye of the mormyrid fish, Gnathonemus petersii

The African weakly electric fish Gnathonemus petersii is well known for its electrosensory capabilities. These animals can detect and distinguish objects through active electrolocation in complete darkness. Because of their nocturnal lifestyle, a low contribution of vision for orientation and object detection has been expected. However, as we show in this review, the retina of G. petersii is highly specialized with hundreds of rods and tens of cones grouped together in bundles in a complex way, ensheathed by a tapetum lucidum. The structure of the bundles goes beyond what would be expected if only photon catch was supposed to be increased. During daytime, the structure of these “macro-receptors” changes dramatically depending on retinomotor movements. During the day, the rods and cones are located in different compartments of the bundle, separated by a narrow canal in the form of a “bottle neck”. Investigations on cell structure and neurochemistry in the retina indicate a general organization that is simpler in terms of bipolar and ganglion cell diversity than in tetrachromatic species such as goldfish, yet similar in terms of neurochemical differentiation of amacrine cells. In both respects, the inner retina of the elephantnose fish bears the greatest similarity to catfish and some deep-sea fish retinae. Neuronal circuits and bundle structure give hints of possible adaptations for contrast and/or movement detection. Behavioral experiments suggest that, in contrast to the vision specialists Lepomis gibbosus, pattern detection of G. petersii is not affected by higher spatial frequencies. A pattern of low spatial frequencies, however, was equally well detected by G. petersii and L. gibbosus. Optomotor response experiments indicate that motion vision is important for Gnathonemus, narrowing down the search for the functional specialization of the Gnathonemus retina and providing a starting point for work on multisensory integration in these fish.     

Modulation of synaptic transfer between retinal cones and horizontal cells by spatial contrast

We studied the influence of steady annular light on the kinetics and sensitivity of horizontal cell (HC) responses to modulation of the intensity of small concentric spots in the turtle retina. As shown by previous investigators, when the intensity of the annulus was equal to the mean spot intensity, spot response kinetics were the same as those for the modulation of spatially uniform light. Turning off the annulus attenuated dramatically high-frequency flicker sensitivity and enhanced somewhat low-frequency sensitivity. This phenomenon reflects a modulation of synaptic transfer between cones and second-order neurons that is mediated by cones, and it will be referred to as cone-mediated surround enhancement (CMSE). Our main results are as follows: (a) The change in test-spot response sensitivity and kinetics upon dimming a steady surrounding annulus is a consequence of the change in spatial contrast rather than change in overall light level. (b) Introduction of moderate contrast between the mean spot intensity and steady surrounding light intensity causes a marked change in spot response kinetics. (c) The dependence of spot response kinetics on surrounding light can be described by a phenomenological model in which the steady state gain and the time constant of one or two single-stage, low-pass filters increase with decreasing annular light intensity (d) The effect of surrounding light on spot responses of a given HC is not determined by change in the steady component of the membrane potential of that cell. (e) Light outside the receptive field of an HC can affect that cell's spot response kinetics. (f) In an expanding annulus experiment, the distance over which steady annular light affects spot response kinetics varies among HCs and can be quite different even between two cells with closely matched receptive field sizes. (g) The degree of CMSE is correlated with HC receptive field size. This correlation suggests that part of the enhancement mechanism is located in the HC. Taken together, our results suggest the involvement of the inner retina in CMSE.     

Changes in the Visual Cell Layer of the Duplex Retina During Growth of the Eye of a Deep-sea Teleost,Gempylus serpens Cuvier, 1829

Ontogenetic changes in the visual cell layer of the duplex retina during growth of the eye of the deep-sea teleost Gempylus serpens, the snake mackerel, are illustrated by comparing the retina of a small specimen with that of a previously studied adult fish. The small specimen has tightly packed cones spanning the whole width of the visual cell layer and small rods situated in its vitread part. Over most of the retina the cone population consists of single cones arranged in a very regular hexagonal mosaic. The temporalmost retina has a cone population consisting mainly of twin cones arranged in meridional rows. Growth of the eye is associated with an increase in the thickness of the visual cell layer and the density of rods and a total elimination of the densely packed single cones, the retina of the adult fish possessing only a temporally located population of double cones. The radical differences between the retina of the small and adult snake mackerel are probably associated with the different light regimes encountered by small and large specimens.