Elena Maximova

Direction Selectivity in the Goldfish Tectum Revisited

Abstract: 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°. 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.

ON THE ORGANIZATION OF RECEPTIVE FIELDS OF ORIENTATION-SELECTIVE UNITS RECORDED IN THE FISH TECTUM

Responses from two types of orientation-selective units of retinal origin (detectors of horizontal lines and detectors of vertical lines) were recorded extracellularly from their axon terminals in the medial sublamina of tectal retinorecipient layer of immobilized cyprinid fish Carassius gibelio. Excitatory and inhibitory influences across receptive fields of orientation-selective units were evaluated. Positions, sizes and forms of the responsive parts of the receptive field were estimated by moving edges and flashing narrow light and dark stripes. It was shown that the orientation-selective units in fish are characterized by small responsive receptive fields with mean width of 4.8 +/- 1.6 degrees (n = 176). The comparison of different types of orientation-selective units revealed that the responsive receptive fields of detectors of vertical lines are significantly wider (13%) than those of detectors of horizontal lines. Statistically significant difference was also found between sizes of responsive receptive fields evaluated by light and dark edges. Mean responsive receptive field width, estimated for light edges (ON responses) were wider than those evaluated for dark edges (OFF responses). Inhibition in the receptive field of orientation-selective units was evaluated on the basis of two experimental methods. Evidence that signals are not linearly summed across the receptive field was derived from experimental results. Inhibitory influences, recorded in the receptive field of orientation-selective units, always initiated inside the responsive receptive field area and spread towards the periphery. Results of the study indicate that receptive fields cannot be defined as homogeneous sensory zone driven by a linear mechanism of response generation. The receptive fields of orientation-selective units, in fish appear to be composed of subunits sensitive to the appropriately oriented stimuli.

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.

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

Abstract: 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.

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.

Photopic Vision in Eels: Evidences of Color Discrimination

Abstract: Several classes of second‐order retinal neurons have been studied electrophysiologically in European eel (Anguilla anguilla) from two different localities, Lake Seliger in Russia and the coastal waters of the Adriatic Sea in Montenegro. The majority of L‐horizontal cells (68 explored) had both rod and cone inputs, an uncommon phenomenon among teleosts. Pronounced color‐opponent properties, often taken as pointing to the capacity of color vision, were identified in one amacrine cell, apparently of the “blue/yellow” (or /blue/green”) type. Microspectrophotometric measurements revealed two different spectral classes of cones with absorption maxima at about 525 and 434 nm. The existence of green‐sensitive and blue‐sensitive cone units was thus revealed by both electrophysiological and microspectrophotometric techniques.

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.

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.

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.