On the organization of receptive fields of retinal spot detectors projecting to the fish tectum: Analogies with the local edge detectors in frogs and mammals.

Responses of ON- and OFF-ganglion cells (GCs) were recorded extracellularly from their axon terminals in the medial sublamina of tectal retino-recipient layer of immobilized cyprinid fish (goldfish and carp). These units were recorded deeper than direction selective (DS) ones and at the same depth where responses of orientation selective (OS) GCs were recorded. Prominent responses of these units are evoked by small contrast spots flickering within or moving across their visual field. They are not selective either to the direction of motion or to the orientation of stimuli and are not characterized by any spontaneous spike activity. We refer to these fish GCs as spot detectors (SDs) by analogy with the frog SD. Receptive fields (RFs) of SDs are organized concentrically: the excitatory center (about 4.5°) is surrounded by opponent periphery. Study of interactions in the RF has shown that inhibitory influences are generated already inside the central RF area. This fact suggests that RFs of SDs cannot be defined as homogeneous sensory zone driven by a linear mechanism of response generation. Physiological properties of fish SDs are compared with the properties of frog SDs and analogous mammalian retinal GCs-local edge detectors (LEDs). The potential role of the SDs in visually guided fish behavior is discussed.

Updated functional segregation of retinal ganglion cell projections in the tectum of a cyprinid fish-further elaboration based on microelectrode recordings.

Single-unit responses of retinal ganglion cells (GCs) were recorded extracellularly from their axonal terminals in the tectum opticum (TO) of the intact fish (goldfish, carp). The depths of retinal units consecutively recorded along the track of the microelectrode were measured. At the depth of around 50 µm, the responses of six types of direction-selective (DS) GCs were regularly recorded. Responses of two types of orientation-selective (OS) GCs and detectors of white and black spots occurred approximately 50 µm deeper. Responses of GCs with dark- and light-sustained activity were recorded deeper than all others, at about 200 µm. The receptive fields of consecutively recorded units overlap, so they analyze the same fragment of the visual scene, focused by eye optic on the photoreceptor raster. The responses of pairs of DS GCs (ON and OFF units that preferred same direction of stimulus movement) and OS GCs (detectors of vertical and horizontal lines) were often simultaneously recorded at one position of the microelectrode. (The paired recordings of certain units amounted about fourth part of all recordings.) This suggests that their axonal arborizations are located close to each other in the tectal retinorecipient layer. Electrophysiological method, thus, allows to indirectly clarify and make precise the morphology of the retino-tectal connections and to establish a morpho-physiological correspondence.

Color properties of the motion detectors projecting to the goldfish tectum.

Interactions between color channels (long-wave (L), middle-wave (M) and short-wave (S)) in the receptive field of direction-selective (DS) and orientation-selective (OS) ganglion cells (GCs) were investigated with combined selective stimulation of pairs of cone types (L and M, L and S, M and S). In the experiments with DS GCs of both ON and OFF types, it was shown that: (1) M and S channels were synergistic relative to each other and opponent to L channel. (2) Three-parameter signal (from L, M and S cones) is transformed to one-parameter signal at the output of DS GC, thus illustrating the principle of univariance. (3) In the experiments with OS GCs, it was shown that L and M channels were synergistic in the OFF-pathway, while the S channel was opponent to them. Our results suggested that photoreceptor synaptic connectivity of the bipolar cells hypothetically involved in the goldfish OS circuitry substantially differs from connectivity of bipolar cells presumably targeting DS GC. (4) To sum up, the results obtained on DS GCs confirmed the plausibility of proposed DS GC wiring diagrams; as to the OS circuitry of fish retina it still remains unclear and needs further investigation.

Color properties of the motion detectors projecting to the goldfish tectum: II. Selective stimulation of different chromatic types of cones.

Sensitivity to the sign of contrast of direction-selective (DS) and orientation-selective (OS) ganglion cells (GCs) was investigated with selective stimulation of different chromatic types of cones. It was shown that the DS GCs that were classified with the use of achromatic stimuli as belonging to the ON type responded to selective stimulation of the long-wave cones as the ON type also, while the stimulation of middle-wave or short-wave cones elicited the OFF type responses. Character of the responses of DS GCs of the OFF type was exactly the opposite. OS GCs, which responded to achromatic stimuli as the ON-OFF type, responded to selective stimulation of the long-wave cones as the ON-OFF type as well, responded to middle-wave stimulation as the OFF type and to stimulation of short-wave cones it responded mainly as the ON type. At the same time, under color-selective stimulation, both DS and OS GCs retained the directional and orientation selectivity with the same preferred directions. The results obtained are in favor of the idea that the signals from the different chromatic types of cones are combined in the outer synaptic layer of the retina at the inputs of bipolar cells using sign-inverting and/or sign-conserving synapses, while specific spatial properties of motion detectors are formed in the inner synaptic layer.

Opposing motion inhibits responses of direction-selective ganglion cells in the fish retina.

Inhibitory influences in receptive fields (RFs) of the fish retinal direction-selective ganglion cells (DS GCs) were investigated. Responses of the fast retinal DS GCs were recorded extracellularly from their axon terminals in the superficial layer of tectum opticum of immobilized fish. The data were collected from two cyprinid species - Carassius gibelio, a wild form of the goldfish, and the barbel fish Labeobarbus intermedius. Visual stimuli were presented to the fish on the monitor screen within a square area of stimulation occupying approximately 11 × 11° of the visual field. DS GCs were stimulated by pairs of narrow stripes moving in opposing directions. One of them entered central (responsive) area of cell receptive field (RRF) from the preferred, and the other one from the null side. Stimuli merged at center of stimulation area, and subsequently moved away from each other. It was shown that the cell response evoked by the stripe coming from the preferred side of RF was inhibited by the stimulus coming from the opposite direction. In the majority of units recorded inhibitory effect induced by the null-side stimulus was initiated in the RF periphery. As a rule, inhibitory influences sent from the RF periphery were spread across the entire central area of RF. Modifications of the inhibitory influences were investigated throughout the whole motion of paired stimuli. Evident inhibitory effects mediated from the null direction were recorded during the approach of stimuli. When stripes crossed each other and moved apart inhibition was terminated, and cell response appeared again. Null-side inhibition observed in fish DS GCs is most likely induced by starburst-like amacrine cells described in morphological studies of different fish species. Possible mechanisms underlying direction selectivity in fish DS GCs are discussed.

Color properties of the motion detectors projecting to the goldfish tectum: I. A color matching study.

Responses of direction-selective and orientation-selective motion detectors were recorded extracellularly from the axon terminals of ganglion cells in the superficial layers of the tectum opticum of immobilized goldfish, Carassius gibelio (Bloch, 1782). Color stripes or edges moving on some color background (presented on the CRT monitor with known emission spectra of its phosphors) served as stimuli. It was shown that stimuli of any color can be more or less matched with the background by varying their intensities what is indicative of color blindness of the motion detectors. Sets of stimuli which matched the background proved to represent planes in the three-dimensional color space of the goldfish. A relative contribution of different types of cones to the spectral sensitivity was estimated according to orientation of the plane of color matches. The spectral sensitivity of any motion detector was shown to be determined mainly by long-wave cones with a weak negative (opponent) contributions of middle-wave and/or short-wave ones. This resulted in reduced sensitivity in the blue-green end of the spectrum, what may be considered as an adaptation to the aquatic environment where, because of the substantial light scattering of a blue-green light, acute vision is possible only in a red region of the spectrum.

Detection and resolution of drifting gratings by motion detectors in the fish retina.

Fish have highly developed vision that plays an important role in detecting and recognizing objects in different forms of visually guided behavior. All of these behaviors require high spatial resolution. The theoretical limit of spatial resolution is determined by the optics of the eye and the density of photoreceptors. However, further in the fish retina, each bipolar cell may collect signals from tens of photoreceptors, and each ganglion cell may collect signals from tens to hundreds of bipolar cells. If we assume that the input signals in this physiological funnel are simply summed, then fine gratings that are still distinguishable at the level of cones should not differ from the homogeneous surface for the ganglion cells. It is therefore generally considered that the resolution of the eye is determined not by the density of cones, but by the density of ganglion cells. Given the size of the receptive field of ganglion cells, one can conclude that the resolving power at the output of the fish retina should be ten times worse than at its input. But this contradicts the results of behavioral studies, for, as it is known, fish are able to distinguish periodic gratings at the limit of resolution of the cones. Our electrophysiological studies with extracellular recording of responses of individual ganglion cells to the motion of contrast gratings of different periods showed that the acuity of ganglion cells themselves is much higher and is close to the limit determined by the density of cones. The contradiction is explained by the fact that ganglion cells are not linear integrators of the input signals, their receptive fields being composed of subunits with significantly smaller zones of signal summation where nonlinear retinal processing takes place.

Cardinal difference between the orientation-selective retinal ganglion cells projecting to the fish tectum and the orientation-selective complex cells of the mammalian striate cortex.

Responses from two types of orientation-selective units of retinal origin were recorded extracellularly from their axon terminals in the medial sublaminae of tectal retinorecipient layer of immobilized cyprinid fish Carassius gibelio. Excitatory and inhibitory interactions in the receptive field were analyzed with two narrow stripes of optimal orientation flashing synchronously, one in the center and the other in different parts of the periphery. The general pattern of results was that the influence of the remote peripheral stripe was inhibitory, irrespective of the polarity of each stripe (light or dark). In this regard, the orientation-selective ganglion cells of the fish retina differ from the classical orientation-selective complex cells of the mammalian cortex, where the remote paired stripes of the opposite polarity (one light and one dark) interact in a facilitatory fashion. The consequence of these differences may be a weaker lateral inhibition in the latter case in response to stimulation by periodic gratings, which may contribute to a better spatial frequency tuning in the visual cortex.

Presynaptic and postsynaptic single-unit responses in the goldfish tectum as revealed by a reversible synaptic transmission blocker.

A variety of visually evoked responses are recorded in the fish optic tectum using single-cell recording technique. Based on indirect criteria (frequency power spectrum of spikes, spike waveform, receptive field size), they may be divided into two groups: those presumably recorded from axon terminals of retinal ganglion cells projecting to the tectum (precynaptic recording), and those recorded from tectal neurons (postsynaptic recording). In the present study, we used cobalt, a reversible blocker of synaptic transmission, as a more crucial criterion to identify the source of these responses. After cobalt application, some units (such as ON- and OFF-types of direction-selective units, orientation-selective and spontaneously active units) were visually responsive, while others (including ON-OFF direction-selective units with large receptive fields) ceased firing. Discrimination of the units by the use of cobalt has been found to coincide with that by the indirect physiological criteria. Thus, the differences in frequency power spectrum of spikes, spike waveform, and receptive field size may be used for efficient and reliable discrimination between pre- and post-synaptic recordings in the fish tectum.

Direction selectivity in the goldfish tectum revisited.

Responses of direction-selective (DS) ganglion cells (GCs) were recorded extracellularly from their axon terminals in the superficial layer of the tectum opticum (TO) of immobilized goldfish, Carassius auratus gibelio (Bloch). Directional tuning curves were measured with contrast edges moving in 12 or more different directions across the receptive field (RF). All directional tuning curves had cardioid-like appearance, their acceptance angles amounted to somewhat more than 180 degrees . According to their preferred directions DS GCs proved to comprise three distinct groups, each group containing DS GCs of ON and OFF subtypes approximately in equal quantity. Thus, this gives six physiological types of DS GCs in total. The preferred direction of a DS GC does not depend to some extent on a value of contrast, speed, size, and form of the stimuli. Coincidence in number of preferred directions with number of semicircular canals implies that DS GCs projecting to tectum are involved in some multimodal sensory integration in postural, locomotor, and oculomotor control in the three-dimensional aquatic world. DS neurons of the TO itself respond independently of the sign of stimulus contrast, have enormous receptive fields, and seem likely to collect signals from the retinal DS units of both ON and OFF subtypes with the same preferred direction.

Spectral sensitivity of direction-selective ganglion cells in the fish retina.

In color matching experiments with extracellular recordings from axon terminals of ganglion cells in the tectum opticum of immobilized goldfish, direction-selective ganglion cells were shown to be color-blind. Their spectral sensitivity is determined by a high positive input from the long wavelength-sensitive cones and weak opponent input from other cone types.