Color- and motion-specific units in the tectum opticum of goldfish.

Extracellular recordings were performed from 69 units at different depths between 50 and [Formula: see text]m below the surface of tectum opticum in goldfish. Using large field stimuli (86[Formula: see text] visual angle) of 21 colored HKS-papers we were able to record from 54 color-sensitive units. The colored papers were presented for 5[Formula: see text]s each. They were arranged in the sequence of the color circle in humans separated by gray of medium brightness. We found 22 units with best responses between orange, red and pink. About 12 of these red-sensitive units were of the opponent "red-ON/blue-green-OFF" type as found in retinal bipolar- and ganglion cells as well. Most of them were also activated or inhibited by black and/or white. Some units responded specifically to red either with activation or inhibition. 18 units were sensitive to blue and/or green, 10 of them to both colors and most of them to black as well. They were inhibited by red, and belonged to the opponent "blue-green-ON/red-OFF" type. Other units responded more selectively either to blue, to green or to purple. Two units were selectively sensitive to yellow. A total of 15 units were sensitive to motion, stimulated by an excentrically rotating black and white random dot pattern. Activity of these units was also large when a red-green random dot pattern of high L-cone contrast was used. Activity dropped to zero when the red-green pattern did not modulate the L-cones. Neither of these motion selective units responded to any color. The results directly show color-blindness of motion vision, and confirm the hypothesis of separate and parallel processing of "color" and "motion".

Visual discrimination of objects differing in spatial depth by goldfish.

Training experiments were performed to investigate the ability of goldfish to discriminate objects differing in spatial depth. Tests on size constancy should give insight into the mechanisms of distance estimation. Goldfish were successfully trained to discriminate between two black disk stimuli of equal size but different distance from the tank wall. Each stimulus was presented in a white tube so that the fish could see only one stimulus at a time. For each of eight training stimulus distances, the just noticeable difference in distance was determined at a threshold criterion of 70% choice frequency. The ratio of the retinal image sizes between training stimulus and comparison stimulus at threshold was about constant. However, in contrast to Douglas et al. (Behav Brain Res 30:37-42, 1988), goldfish did not show size constancy in tests with stimuli of the same visual angle. This indicates that they did not estimate distance, but simply compared the retinal images under our experimental conditions. We did not find any indication for the use of accommodation as a depth cue. A patterned background at the rear end of the tubes did not have any effect, which, however, does not exclude the possibility that motion parallax is used as a depth cue under natural conditions.

General principles in motion vision: color blindness of object motion depends on pattern velocity in honeybee and goldfish.

Visual systems can undergo striking adaptations to specific visual environments during evolution, but they can also be very "conservative." This seems to be the case in motion vision, which is surprisingly similar in species as distant as honeybee and goldfish. In both visual systems, motion vision measured with the optomotor response is color blind and mediated by one photoreceptor type only. Here, we ask whether this is also the case if the moving stimulus is restricted to a small part of the visual field, and test what influence velocity may have on chromatic motion perception. Honeybees were trained to discriminate between clockwise- and counterclockwise-rotating sector disks. Six types of disk stimuli differing in green receptor contrast were tested using three different rotational velocities. When green receptor contrast was at a minimum, bees were able to discriminate rotation directions with all colored disks at slow velocities of 6 and 12 Hz contrast frequency but not with a relatively high velocity of 24 Hz. In the goldfish experiment, the animals were trained to detect a moving red or blue disk presented in a green surround. Discrimination ability between this stimulus and a homogenous green background was poor when the M-cone type was not or only slightly modulated considering high stimulus velocity (7 cm/s). However, discrimination was improved with slower stimulus velocities (4 and 2 cm/s). These behavioral results indicate that there is potentially an object motion system in both honeybee and goldfish, which is able to incorporate color information at relatively low velocities but is color blind with higher speed. We thus propose that both honeybees and goldfish have multiple subsystems of object motion, which include achromatic as well as chromatic processing.

Rod-cone based color vision in seals under photopic conditions.

Marine mammals have lost the ability to express S-cone opsin, and possess only one type of M/L-cone in addition to numerous rods. As they are cone monochromats they should be color blind. However, early behavioral experiments with fur seals and sea lions indicated discrimination ability between many shades of grey and blue or green. On the other hand, most recent training experiments with harbor seals under "mesopic" conditions demonstrated rod based color blindness (Scholtyssek et al., 2015). In our experiments we trained two harbor seals (Phoca vitulina) and two South African fur seals (Arctocephalus pusillus) with surface colors under photopic conditions. The seals had to detect a triangle on grey background shown on one of three test fields while the other two test fields were homogeneously grey. In a first series of experiments we determined brightness detection. We found a luminance contrast of >3% sufficient for correctly choosing the triangle. In the tests for color vision the triangle was blue, green or yellow in grey surround. The results show that the animals could see the colored triangle despite minimal or zero brightness contrast. Thus, seals have color vision based on the contribution of cones and rods even in bright daylight.

Wavelength dependence of the optomotor response in zebrafish (Danio rerio).

The action spectrum of motion detection in zebrafish (Danio rerio) was measured using the optomotor response in the light adapted state. The function has a single maximum at 550-600 nm, and is similar to the spectral sensitivity function of the L-cone type in the mid and long wavelength range. At shorter wavelengths the values of three of the five fish tested are lower. As in goldfish [Vis. Res. 36 (1996) 4025], the result indicates a dominance of the L-cone type with an inhibitory influence of M- or S-cones. Experiments with a red/green striped cylinder showed that the optomotor response was at minimum whenever the L-cone type was not modulated by the moving pattern. This demonstrates that motion vision in zebrafish is "color blind", using mainly one of the four cone types probably involved in color vision.

Neuropharmacology of vision in goldfish: a review.

The goldfish is one of the few animals exceptionally well analyzed in behavioral experiments and also in electrophysiological and neuroanatomical investigations of the retina. To get insight into the functional organization of the retina we studied color vision, motion detection and temporal resolution before and after intra-ocular injection of neuropharmaca with known effects on retinal neurons. Bicuculline, strychnine, curare, atropine, and dopamine D1- and D2-receptor antagonists were used. The results reviewed here indicate separate and parallel processing of L-cone contribution to different visual functions, and the influence of several neurotransmitters (dopamine, acetylcholine, glycine, and GABA) on motion vision, color vision, and temporal resolution.

Perception of illusory surfaces and contours in goldfish.

Goldfish (Carassius auratus) were trained to discriminate triangles and squares using a two choice procedure. In the first experiment, three goldfish were trained with food reward on a black outline triangle on a white background, while a black outline square was shown for comparison. In transfer tests, a Kanizsa triangle and a Kanizsa square were presented, perceived by humans as an illusory triangle- or square-shaped surface of slightly higher brightness than the background. The choice behavior in this situation indicates that goldfish are able to discriminate between both figures in almost the same way as in the training situation. In control experiments goldfish did not discriminate between shapes in which humans do not perceive the illusion. A series of generalization experiments was performed indicating the similarity between the tested shapes and the training triangle. From all these findings we conclude that goldfish are able to perceive an illusory triangle or square within the Kanizsa figures. In a second experiment, four goldfish were trained on a white outline triangle versus a white outline square, both on black background with white diagonal lines. In transfer tests in which the shapes were replaced by gaps within the white diagonal lines, goldfish were clearly able to discriminate between the two patterns based on the illusory contours. This was not the case in transfer tests with phase shifted abutting lines.

Small field motion detection in goldfish is red-green color blind and mediated by the M-cone type.

Large field motion detection in goldfish, measured in the optomotor response, is based on the L-cone type, and is therefore color-blind (Schaerer & Neumeyer, 1996). In experiments using a two-choice training procedure, we investigated now whether the same holds for the detection of a small moving object (size: 8 mm diameter; velocity: 7 cm/s). In initial experiments, we found that goldfish did not discriminate between a moving and a stationary stimulus, obviously not taking attention to the cue "moving." Therefore, random dot patterns were used in which the stimulus was visible only when moving. Using black and white random dot patterns with variable contrast between 0.2 and 1, we found that the fish could see motion only with high (0.8) contrast. In the decisive experiment, a red-green random dot pattern was used. By keeping the intensity of the red dots constant and reducing the intensity of the green dots, a narrow intensity range was found in which goldfish could no longer discriminate between the moving random dot stimulus in random dot surround and the stationary random dot pattern. The same was the case when a red moving disk was presented in green surround. This is the evidence that object motion is red-green color blind, i.e., color information cannot be used to detect the moving object. Calculations of the cone excitation values revealed that the M-cone type is decisive, as this cone type (and not the L-cone type) is not modulated by that particular red-green pattern in which the moving stimulus was invisible.

Generalization and categorization of spectral colors in goldfish. II. Experiments with two and six training wavelengths.

In part I of this study (Kitschmann and Neumeyer 2005), goldfish categorized spectral colors only in the sense that wavelengths in a range of about twice as large as the just noticeable difference were treated as similar to a given training wavelength. Now, we trained goldfish on more than one wavelength to prevent very accurate learning. In one experiment goldfish were trained on six adjacent wavelengths with equal numbers of rewards, and, thus, equal numbers of learning events. Generalization tests showed that some wavelengths were chosen more often than others. This indicated that certain spectral ranges are either more attractive or more easily remembered than others. As this is a characteristic of the "focal" colors or centers of color categories in human color vision, we interpret the findings in goldfish accordingly. We conclude (Figs. 5 and 6) that there are four categories in spectral ranges approximately coinciding with the maximal sensitivities of the four cone types, and three categories in-between. Experiments with two training colors indicate that there is no direct transition between categories analogous to human "green" and "red", but that there is a color analogous to human "yellow" in-between (Figs. 2, 3; Table 1).

Generalization and categorization of spectral colors in goldfish I. Experiments with one training wavelength.

Goldfish have a tetrachromatic color vision with a high discrimination ability for spectral colors as well as for object colors. We investigate the question whether goldfish organize the high number of discriminable colors in terms of color categories, i.e. in a few larger groups of colors independent of wavelength discrimination. Twenty-four goldfish were trained with food reward, each fish on one out of 13 wavelengths between 371 nm and 630 nm. In transfer tests two different wavelengths were presented, one shorter and one longer than the training wavelength, and the choice behavior was determined. Choice frequencies of >or=50% were assumed to indicate similarity to the training color. The wavelength ranges >or=50% were about 100 nm and twice as large as the just noticeable differences measured in wavelength discrimination tests (Fig. 7). The ranges were surprisingly about the same for all training wavelengths, provided the data were plotted on a wavelength scale weighted according to discrimination ability (Fig. 4). Thus, with the training method chosen goldfish showed a kind of categorization which, however, depends on training wavelength and discrimination ability. Generalization tests in which training wavelength and test wavelengths were shown separately for 2 min each gave the same results as wavelength discrimination tests (Figs. 5 and 6) and are, therefore, not indicative for color categories.

Simultaneous and successive colour discrimination in the honeybee (Apis mellifera).

The colour discrimination of individual free-flying honeybees (Apis mellifera) was tested with simultaneous and successive viewing conditions for a variety of broadband reflectance stimuli. For simultaneous viewing bees used form vision to discriminate patterned target stimuli from homogeneous coloured distractor stimuli, and for successive discrimination bees were required to discriminate between homogeneously coloured stimuli. Bees were significantly better at a simultaneous discrimination task, and we suggest this is explained by the inefficiency with which the bees' brain can code and retrieve colour information from memory when viewing stimuli successively. Using simultaneous viewing conditions bees discriminated between the test stimuli at a level equivalent to 1 just-noticeable-difference for human colour vision. Discrimination of colours by bees with simultaneous viewing conditions exceeded previous estimates of what is possible considering models of photoreceptor noise measured in bees, which suggests spatial and/or temporal summation of colour signals for fine discrimination tasks. The results show that when behavioural experiments are used to collect data about the mechanisms facilitating colour discrimination in animals, it is important to consider the effects of the stimulus viewing conditions on results.

Honeybee (Apis mellifera) vision can discriminate between and recognise images of human faces.

Recognising individuals using facial cues is an important ability. There is evidence that the mammalian brain may have specialised neural circuitry for face recognition tasks, although some recent work questions these findings. Thus, to understand if recognising human faces does require species-specific neural processing, it is important to know if non-human animals might be able to solve this difficult spatial task. Honeybees (Apis mellifera) were tested to evaluate whether an animal with no evolutionary history for discriminating between humanoid faces may be able to learn this task. Using differential conditioning, individual bees were trained to visit target face stimuli and to avoid similar distractor stimuli from a standard face recognition test used in human psychology. Performance was evaluated in non-rewarded trials and bees discriminated the target face from a similar distractor with greater than 80% accuracy. When novel distractors were used, bees also demonstrated a high level of choices for the target face, indicating an ability for face recognition. When the stimuli were rotated by 180 degrees there was a large drop in performance, indicating a possible disruption to configural type visual processing.

Colour constancy in goldfish and man: influence of surround size and lightness.

Colour constancy was investigated by using a series of 10 simultaneously presented surface colours ranging in small steps from green through gray to red-purple. Goldfish were trained to select one medium test field when the entire setup was illuminated with white light. In the tests, either red or green illumination was used. Colour constancy, as inferred from the choice behaviour, was perfect under green illumination when the test fields were presented on a gray or a white background, but imperfect on a black background. Under red illumination and a white background, however, colour constancy was overcompensated. Here, a colour contrast effect was observed. The influence of background lightness was also found when the surround was restricted to a narrow annulus of 4-11 mm width (test field diameter: 14 mm). By applying colour metrics it could be shown that the von Kries coefficient law can describe the overall effect of colour constancy. For an explanation of the effect of surround size and lightness, lateral inhibitory interactions have to be assumed in addition, which are also responsible for simultaneous colour contrast. Very similar results were obtained in experiments with the same colours in human subjects. They had to name the test field appearing 'neutral' under the different illumination and surround conditions, as tested in the goldfish experiment.