Vision in toads
The neural basis of prey detection, recognition, and orientation was studied in depth by Jörg-Peter Ewert in a series of experiments that made the toad visual system a model system in neuroethology. He began by observing the natural prey catching behavior of the common European toad.
Ewert's work studying toads yielded several important discoveries. In general, his research revealed the specific neural circuits for recognition of complex visual stimuli. Specifically, he identified two main regions of the brain, the optic tectum and the pretectal caudal thhalamic region, that were responsible for discriminating prey from non-prey and revealed the neural pathways that connect them. Furthermore, he found that the neural mechanisms are plastic and adaptable to varying environments and conditions.
Natural toad behavior
Vision in toads is a complex matter. Toads respond to objects depending on: a) what they see where the object is located in the visual field the toad's motivation, i.e. its interest, which can be influenced by endogeneous factors such as hunger, the time of day, and season, as well as event-related individual experiences.The annual life cycle of common toads is divided into different seasonal periods: winter for hibernation, spring for mating, summer for prey hunting as well as threat avoiding, and fall for migration to wintering grounds. In the context of a main season, behavioral objectives and their underlying motivations are commensurate. However, a high level of motivation can substantially influence the attribution of a visual object to a particular meaning category and vice versa. For instance, during the mating season, visual prey objects are ignored by toads. Male common toads are attracted to the large swollen bodies of their females, which are suitable for clasping and carrying a male on their back. In the event of a male, driven by testosterone eager to mate cannot find a female in the pond quickly, it will even utilize an oversize piece of floating tree bark as a substitude by intensely clasping it.
During the hunting season, the common toad responds to a moving insect or worm with a series of prey-catching reactions: orienting towards prey, stalking up to prey, binocular fixation, snapping, swallowing and mouth-wiping with forelimb. The sequence of reactions to forms a kind of stimulus-response chain in which the prey-signal, in combination with a new location-signal, determines the stimulus constellation for the next type of reaction: When an object is recognized as prey and thus attracts attention, and the prey is in the peripheral field of vision, the toad turns its head and body toward the prey. If the prey is far away, the toad begins to pursue it. After reaching the prey, the toad fixes its gaze on it intensely with both eyes. Finally, it snaps at prey from short distance with its tongue or jaws. These stimulus responses form a series of clearly defined behavioral patterns.
One reason for this type of stimulus-response chain is that, unlike humans, toads do not have involuntary saccadic eye movements, and they also cannot perform "tracking eye movements". Their visual system, therefore, focuses on the perception of retinal images of moving visual objects. Furthermore, they depend on recognizing the visual stimulus before they respond behaviorally. As a result, they have developed a specific detection system that, for example, allows them to discriminate between live prey and dangerous predators. Since common toads Bufo bufo bufo are mainly active at dusk and dawn, a question of color vision was not the focus of the quantitative studies of their visually controlled behavior.
The lack of saccadic eye movements forces the toad to hold its eyes in rigid positions. Therefore, it must decide whether the object is "prey" or "non-prey" before moving itself. If it orients towards an object, it must already have decided "prey" and then commits itself to snapping by reducing the thresholds for subsequent prey-catching responses. Even when the prey stimulus quickly disappeared after orienting, the aroused toad may sometimes complete the subsequent responses.
Prey vs. predator response
Among potential prey, common toads prefer small invertebrates that move in the direction of their body axis, such as ants, snails, beetles, millipedes, and worms. They avoid large, moving objects such as the shadows of birds of prey or objects whose body parts are aligned perpendicular to the direction of movement, such as snakes or certain caterpillars. When a toad is presented with a moving stimulus, it generally may react with one of two responses: Depending on the size and the configuration of the stimulus, it will either engage in prey orienting behavior or predator avoidance behavior, which consists of ducking-down postures or jumping away in panic. Snakes are considered the arch enemies of toads. Snakes move in a way that toads perceive as a warning: the snake raises its head and moves its body coils sideways, hence creating images that run transverse to the direction of motion. This dynamic gestalt contrasts with that of an earthworm, for example, and is therefore referred to in laboratory jargon as anti-worm configuration vs. worm configuration. When confronted by a horseshoe whip snake, the toad will crouch down and try to dig in, jump away, or remain motionless. Sitting still, it employs various defense strategies while maintaining eye contact and secreting poison from its skin glands. Its body swells, causing it to assume a defensive stance with its head lowered and legs extended. At the same time, its head and back serve as a protective shield. This posture puts the toad in a position that makes it difficult for a snake to attack or grab it.In determining the overall size of a stimulus, a toad will consider both the angular size, which is measured in degrees of visual angle, and the absolute size, which takes into consideration the distance between the toad and the object. This second ability, to judge absolute size by estimating distance, is known as size constancy.
To study behavioral responses of toads to varying types of stimuli, Ewert conducted experiments by placing the toad in the center of a little cylindrical glass vessel. He then rotated a small stripe of contrasting cardboard around the vessel to mimic either prey-like or threat-like stimuli; . The rate of turning was recorded as a measure of orienting behavior. By changing characteristics of the visual stimulus in a methodical manner, Ewert was able to comprehensively study the key features that determine behavior.
Up to a certain size, squares rotating around the toad successfully elicited prey-catching responses. Toads avoided large squares. Vertical bars nearly never elicited prey-catching behavior, and they were increasingly ineffective with increasing height. Horizontal bars, in contrast, were very successful at eliciting prey-catching behavior and their effectiveness increased with increasing length, to a certain degree. Additional vertical segments on top of horizontal bars significantly decreased prey-catching responses. By means of a different experimental setup it was shown that the worm vs. anti-worm discrimination is independent of the direction the object moves in the toad's visual field. Taking into account motion direction invariance, a more general formulation is: alignment of a bar parallel to vs. transverse its direction of motion. The movement specificity of the toad's visual system is instrumental for classifying moving visual objects as prey or threads. This classification is based on a calculation of the alignment of the longitudinal axes of the objects in relation to the direction of their motion, as opposed to gravity as a reference value : A millipede running horizontally along the ground or climbing up a vertical blade of grass falls into the toad's prey category. For models of prey vs. threat recognition, see: concept of 'neural filter interaction'; 'systems theoretical analysis'; 'schema theoretical approach'.
A stationary object, such as a barrier, elicits evasive detour behavior of the toad. However, there are examples showing that stationary objects under certain conditions trigger prey capture: When a toad moves its head with its immobile eyes, the retinal image of an object moves in the opposite direction due to induced movement. It is recognized as prey and responded to with prey capture, provided the configuration of the image matches the prey schema of the analyzing central visual system. This applies when the background of the object is untextured, e.g. a black object in front of a white background. However, if the background is textured, such as by a Julesz random-dot texture or a natural view of a forest floor with little branches and leaf structures, the object is ignored by the toad due to visual masking: The object is masked by the moving background texture. The inhibitory phenomenon between the target stimulus and the masking stimulus was investigated in toads quantitatively using various experimental procedures.
Furthermore, the direction of the contrast between stimulus and background can significantly affect the type of behavior: In response to a wormlike stripe, common toads orient and snap towards the edge leading in the direction of motion, given that the stripe is black and the background white. If the stimulus/background contrast is reversed, the toad prefers the trailing edge of the white stripe and often snaps behind it. Obviously, "off"-effects by the moving contrast borders play a guiding role. Generally, white square objects moving against a black background are more attractive as prey than black objects of the same size and configuration against a white background. However, this tendency is plastic and reverses seasonally.
Feature detectors and the visual system
Selected functions of the toad‘s visual system:1.) The neural circuitry mediating between configurational features of the visual prey stimulus and prey capture behavior consists of retina-fed tectal pathways and corresponding rhombencephalic/spinal nuclei.
2.) The distinction between prey and non-prey is based on network interaction of the retino-tectal pathways of the mesencephalon with retino-pretectal thalamic structures of the diencephalon.
3.) The localization of moving visual objects takes advantage of the retinotopic map in the optic tectum in connection with monocular and binocular depth calculations and retino-tectal/tegmental patways.
4.) Targeted attention, i.e., the translation of visual perception into motor action, is based on disinhibitory modulating forebrain loops involving the telencephalic striatum.
5.) Modification of configurational prey recognition in the course of visual or olfactory associative learning are based on a modulating disinhibitory forebrain loop involving the telencephalic posterior ventromedial pallium, the anterior thalamus, the pretectal caudal dorsolateral thalamus and the optic tectum.
6.) Dopaminergic modulations in the brain's macronet increase firing rates of retinal ganglion cells and the preying motivation and alter capture strategies with regard to pursuing and hunting prey versus waiting for prey and snapping.
File:Toad-prey-feature- detectors.jpg|thumb|Tectal prey feature detectors T5.2 project the axons towards bulbar premotor/motor systems. Their response characteristic results from integration in a neuronal network involving retinal ganglion cells R2, R3, R4, pretectal caudal thalamic neurons TH3, and tectal neurons T5.1, T5.2, T5.3. Arrows: excitatory connections; lines with terminal dots: inhibitory influences suggested: presynaptic inhibition and postsynaptic inhibition via inhibitory tectal T5.3 interneurons. Connections were checked, e.g., by means of intracellular recording postsynaptic potentials, horseradish peroxidase or cobalt-lysine backfilling, antidromic electro-stimulation/recording, neurochemical techniques, chemical lesions by kainic acid. Hypothesis after Ewert 1974 and 2004
To understand the neural mechanisms underlying the toad's behavioral responses, Ewert performed a series of recording and visual stimulation experiments. First and foremost, the results allowed him to understand the way the visual system is constructed and connected to the [central nervous system. Secondly, he discovered areas of the brain that were responsible for differential analysis of visual stimuli.
The retina is connected to the optic tectum by at least three types of ganglion cells, each with an excitatory receptive field and a surrounding inhibitory receptive field, but they differ in the diameters of their central excitatory receptive fields, ERF, and the inhibitory receptive fields, IRF. The ERF-diameters in class II ganglion cells are approximately four degrees visual angle. Those in class III cells are about eight degrees, and ERFs of class IV ganglion cells range from twelve to fifteen degrees. As stimuli move across the toad's visual field, information is sent to the optic tectum in the toad's midbrain. The optic tectum exists as an ordered localization system, in the form of a topographical map. Each point on the map corresponds to a particular region of the toad's retina and thus its entire visual field. Likewise, when a spot on the tectum was electrically stimulated, the toad would turn toward a corresponding part of its visual field, as if this part was stimulated by a prey object, hence providing further evidence of the direct spatial connections.
Among Ewert's many experimental goals was the identification of feature detectors, neurons that respond selectively to specific features of a sensory stimulus. Results showed that there were no "worm-detectors" or "enemy-detectors" at the level of the retina. Instead, he found that the optic tectum and the pretectal caudal thalamic region play significant roles in the analysis and interpretation of visual stimuli.
Electrical stimulation experiments demonstrated that the optic tectum initiates orienting and snapping behaviors. It contains many different visually sensitive neurons, among these type I and type II neurons. Type I neurons are activated when an object traversing the toad's visual field is extended parallel to the direction of movement; type II neurons, too, but they will fire less when the object is extended across the direction of movement. Those T5.2 neurons display prey-selective properties; see prey feature detectors. The discharge patterns of these neurons – recorded in freely moving toads – "predict" prey-catching reactions, e.g., the tongue flip of snapping. Their axons project down to the bulbar/spinal motor systems, such as the hypoglossal nucleus which harbors the motor neurons of the tongue muscles. In combination with additional projection neurons, prey-selective T5.2 cells contribute to the ability of the tectum to initiate orienting behavior and snapping, respectively.
The caudal thalamic region initiates avoidance behaviors in the toad. More specifically, electrical triggering this region initiates a variety of protective movements, such as eyelid closing, ducking, and turning away. Various types of neurons in this region are responsible for the avoidance behaviors, and they are all sensitive to different types of visual stimuli: One type of neurons is activated by large, moving objects and — in the case of bar stimuli — those that are aligned across the direction of movement. Another type is activated by a looming object moving toward the toad. Still other types respond to large stationary obstacles, and there are also neurons responding to stimulation of the balance sensors in the toad's ear. Stimulation of such types of neurons would cause the toad to display different kinds of protective behaviors.
Lesioning experiments led to the discovery of pathways extending between the optic tectum and the pretectal thalamic region. When the tectum was removed, prey-orienting behavior disappeared. When the pretectal thalamic region was removed, avoidance behavior was entirely absent while prey-orienting behavior was enhanced even to predator objects. Prey-selective properties were impaired both in prey-selective T5.2 neurons and in prey-catching behavior. Finally, when one side of the pretectal thalamic region was removed, the disinhibition of prey-catching applied to the entire visual field of the opposite eye. These and other experiments suggest that pathways, involving axons of type TH3 threat-feature detectors —which are also retinotopically mapped— extend from the pretectal thalamus to the map of the optic tectum, suitable to modulate tectal responses to visual stimuli and to determine prey-selective T5.2 properties due to inhibitory influences. During intracellular recordings from frog’s tectal neurons in response to pretectal stimulation, about 98% of the implated cells showed inhibitory responses.
Modulatory loops, ontogenetic specifications, and evolutionary perspectives
Having analyzed neuronal processing streams in brain structures that mediate between visual stimuli and adequate behavioral responses in toads, Ewert and coworkers examined various neural loops that—in connection with certain forebrain structures —can initiate, modulate or modify stimulus-response mediation. For example, in the course of associative learning, the toad's visual prey schema can be modified to include non-prey objects. The application of the -2DG method showed that the telencephalic posterior ventral medial pallium vMP revealed a significant increase in metabolic activity in the conditioned toads during prey capture toward large moving objects they had avoided prior to associative conditioning. After lesions to vMP, the conditioning effects of the toads failed, and their recognition of prey demonstrated species-specificity with the selectivity presumed to be phylogenetically conservedThe posterior part of the ventromedial pallium is homologous to the hippocampus of mammals which is also involved in learning processes. Both in anuran amphibians and mammals striatal efferents are involved in directed attention, i.e. gating an orienting response towards a sensory stimulus. The anuran striatum is homologous to a portion of the amniote basal ganglia.
From an evolutionary point of view, it is important to note that the tetrapod vertebrates share a common pattern of homologous forebrain and brainstem structures. Neuroethological, neuroanatomical, and neurochemical investigations suggest that the neural networks underlying essential functions—such as attention, orienting, approaching, avoidance, associative or non-associative learning, and basic motor skills—have, so to speak, a phylogenetic origin in homologous structures of the amphibian brain. Detlev Ploog and Peter Gottwald open a discussion in evolutionary psychology whether heading towards something or heading away from something—in a general sense— might have their primordial roots in diencephalic and mesencephalic nuclei of amphibians.
From a neural network approach, it is reasonable to ask how the toad's ability to classify moving objects by special configuration cues develops, and whether this is unique in the animal kingdom. Developmental studies suggest that the detection principle is an adaptation in amphibians to their biotope and life style.
After hatching from the egg, the tadpole of Bufo bufo is programmed for a life in water and the subsequent postmetamorphic transition to life on land. To achieve this, hormonal, neural, neurosensory, and sensorimotor adaptations take place. The feeding behavior of the tadpole—which consumes bacteria and algae on aquatic plants, as well as carrion and debris—shifts during metamorphosis to a predatory, carnivorous lifestyle. This change goes hand in hand with a selectivity for visual prey objects that ‘move’ and thus show that they are alive and different from the stationary surround. An important discovery, therefore, is that common toads are predisposed to hunt worm-like moving objects in a configuration whose extension parallel to the direction of motion is typically greater than the extension transverse to it, and to avoid objects as threat that occur in anti-worm configuration. The ‘worm preference‘ is established after metamorphosis—during the toad's first steps on land—without it having to learn, and this preference matures over time.
The discrimination between prey and predator and the hunting behavior of toads towards the end of metamorphosis therefore require a redesign of visual perception with regard to the necessary neural and sensorimotor functions: The motion specificity of retinal R2 neurons contributes to the excitability of tectal T5.1 neurons in response to spatiotemporal features of contrast borders of objects aligned with their direction of motion. Since the neural discharge rates increase with the increasing edge length of an object, its trigger values for activating prey capture also increase. This, in turn, would mean the risk of neuronal avalanche excitation due to intratectal recurrent excitation if there were no inhibitory neuronal counteraction. Based on the brain development of Discoglossus frog tadpoles, it is assumed that during metamorphosis at Taylor&Kollros-stage-X optical morphogenetic influences from the optic tectum to the adjacent caudal dorsomedial thalamus initiate a parcellation process of segregation. The new aggregate is called the dorsolateral area. It is thought to contain retino-receptive neurons, which—like TH3 cells in adult toads—are known to control the excitation of the optic tectum through massive inhibitory influences along their axons, similar to what is observed in frogs. The thalamic TH3 cells with input of retinal R3- neurons of the toad are sensitive to contrast borders that are aligned transversely to their direction of movement, thereby limiting tectal excitation in a finely tuned manner that simultaneously determines the prey selectivity of tectal T5.2 neurons.
The tectal avalanche hypothesis in common toads Bufo bufo bufo is substantiated by results of a lesion in the pretectal caudal dorsal thalamus. Experimentally, when the surfaces of the various standard worm, anti-worm, and square test objects were stepped up in size, the tectal neuronal T5.1;2 responses of the brain lesioned toad and its prey-catching reactivity increased progressively all in the same way.
This lesion eliminated the toad's ability to distinguish between objects of different configurations and thus to correctly assign moving visual objects to a category of meaning, either prey or threat. Every moving object triggered a sometimes intense reflexive mouth behavior in the toad — a kind of prey object tracking and prey-oriented empty snapping — even in the direction of its moving hind feet.
If the retina-fed caudal dorsolateral thalamic region, which is tiny compared to the volume of the retina and the optic tectum, loses its control over retino-tectal information processing, the toad’s visual system collapses—in the broadest sense, comparable to visual agnosia.
File:Model2.18.01.26.png|thumb|Working hypothesis on the control of toad’s pretectal thalamus in connection with associative conditioning. R, retina; R2,3,4, classes of retinal ganglion cells; TH3 pretectal thalamic neurons; TH4, predator selective neurons; T5.1, tectal filter neurons; T5.2, prey selective tectal neurons; T5.3, tectal inter neurons; vMP, posterior medial pallium; aTH, anterior thalamus; line with arrow: excitatory influence; line with cross bar: inhibitory influence. The activity pattern considers the changes in metabolic glucose utilization during prey capture of a toad in response to a large moving square object after hand-feeding conditioning: The -2DG uptake in vMP and optic tectum increased, while uptake in pretectal dorsomedial/lateral thalamus decreased. This does not exclude differerent telencephalo-tectal disinhibitory processing streams. Further explanations see text. Adapted from Ewert 1974 and 1997
Large threatening objects stimulate pretectal thalamic TH3 and tectal T5.1 neurons to activate the threat avoidance channel. The question arises: What controls the pretectal dorsal thalamus? We recall the experiments on conditioning with hand feeding: The toad’s species-specific ability to recognize prey, can be modified by individual experience. A simplified working hypothesis suggests why toads after associative conditioning classify a large moving object as prey, much like following a pretectal thalamic lesion.
During the training phase, the experimenter presented a mealworm with hand to the toad once a week for two weeks. It is assumed that at the same time, a subliminal prey signal from the neuronal prey-catching channel AND a subliminal threat signal from the threat-avoidance channel were paired in hypothetical neurons of the telencephalic posterior pallium, vMP. Such pallial cells become sensitized after a period of the prey-threat pairing and thus can be activated by a stimulus from one of the two channels: prey OR threat. The pallial cells — via the anterior thalamus — are suggested to inhibit threat-detecting TH3 cells of the pretectal dorsolateral thalamus, thereby interrupting the threat channel, and disinhibiting prey-detecting T5.2 cells, thereby channeling the prey channel:
Disinhibitory pathway
vMP–> aTH–/ TH3–/ T5.2–> disinhibiting prey capture
The T5.2 cells expand their configurative response spectrum and include visually threatening objects as prey, which is reflected in corresponding prey capture activity. Experimental test of the pallial influence: After vMP lesion, the species-specific prey selectivity in toad's prey capture behavior is re-established. Disinhibition in neuronal networks is defined as a temporary inhibition brake that promotes excitation. This evolutionary conserved circuit is implicated in different functions, including sensory processing, learning, and memory.
Experiments, in which the olfactory non-prey stimulus cineol was combined with a visual prey stimulus during prey capture, showed that the toad's configurative prey selectivity for the moving test objects was expanded in the presence of the conditioned stimulus cineol. However, that kind of expansion resulted from an olfactory stimulus transmitted by the main olfactory bulb, associated with a visual signal in the medial pallium, passing the ventral hypothalamus, and arriving back in the optic tectum. This influenced the level of prey motivation as it served to decrease a visual threshold to the readiness of preying. The prey-oriented behavior toward the test objects was similar to the behavior observed after visual threat/prey conditioning or after a lesion to the pretectal thalamus.
As for the recovery effects after visual threat/prey conditioning, the species specificity was fully restored immediately following a vMP lesion, but selectivity recovered only slowly over time without such a brain lesion. After the expansion of prey selectivity due to a pretectal thalamic lesion, species specificity recovered to a certain extent after 5 days, probably due to intrinsic functional recovery, but without reaching its original selectivity in the following 10 days.
The significant role of pretecto-tectal inhibitory connections for visual configurational pattern recognition and associative learning in toads raises the question of the kind of neurotransmission. Various authors suggest that pretectally released neuropeptide Y via Y2 receptor has an evolutionarily conserved function in the modulation of visual information processing in tetrapods and may exhibit plasticity with regard to neural restructuring during phylogenetic development, for example, with regard to differences in visual pattern discrimination by modifiable release mechanisms.
Behavioral studies showed that the fire-bellied toad disregarded a worm-like prey dummy of black cardboard when the object traversed the visual field of toad‘s tectal lobe, on the surface of which porcine NPY had been administered, soaked in an agarose gel-pad. As this prey object passed through the visual field of the untreated tectal lobe, which was covered with a gel-pad soaked with frog-Ringer without NPY, it released prey capture. Comparable experiments measuring metabolic activity confirmed a difference in -2DG uptake in dorsal tectal layers between the NPY-treated and untreated tectal lobes. That is consistent with studies in cane toads in which excitatory tectal field potentials in response to electrical stimulation of the contralateral optic nerve were attenuated by NPY-application to the tectal surface. Fact is also that pretecto-tectal projections in frogs – originating ipsilaterally from pretectal dorsomedial and dorsolateral thalamic nuclei – release NPY which in turn suggests that NPY exerts an inhibitory influence on retino-tectal transmission: If electrical stimulation of the ipsilateral pretectal dorsomedial/lateral thalamus preceded an optic nerve stimulation by a delay of 15 ms, the excitatory tectal field potential to optic nerve stimulation was strongly attenuated. This allows the conclusion that NPY — released from pretecto-tectal projecting fiber terminals and signaling through Y2 receptor — acts presynaptically on retino-tectal terminals to inhibit glutamate mediated retino-tectal transmission. In fact, spike amplitudes of retino-tectal projecting R2 and R3 ganglion cells in response to moving visual objects were reduced under NPY influence to the superficial tectal layers, thus leading to a reduced release of glutamate.
The pretectal thalamic TH3 and TH4 neurons of the toad's visual system are attributed the following main functions: i) Detection of a large moving threat object and, specifically, a contrast boundary aligned transverse to the direction of its motion; ii) adaptive, configuration-dependent scaling and categorization of moving visual objects through computations and in interaction with T5.1 and T5.2 neurons, as well as producing behavioral trigger thresholds that result in sensorimotor decisions; iii) a finely tuned modulation of inhibitory processes within the optic tectum.
An important feature of movement specificity in toad vision is the “implicit computation” of contrast borders in relation to the direction of their movement. This can be regarded as a ‘trick‘ by which anuran brain evolution circumvents the need of a huge number of visual neurons with ‘asymmetric‘ receptive fields in order to “explicitly compute“ various possible contrast boundaries, as known from the visual cortex. In toads, an apparently equivalent solution is achieved by T5.2 and TH3 cells, whose excitatory receptive fields are ‘radially symmetric‘, thus enabling the calculation of contrast borders implicitly with respect to any direction of motion. That too shows how a small brain with limited neuroarchitecture can solve a hardware problem with the help of its intelligent software.
Comparable detection principles are discovered in amphibious fish and in insects. In mammals, erect body postures, for example, may address a threat signal to a rival. In humans, the gesture of a vertically oriented, horizontally waving index finger is worth mentioning. Depending on the context, this gesture can be interpreted as either a threatening or warning gesture in the biological sense. For instance, it can precede an attack or serve as a deterrent. The ritualization of behaviors is defined as stereotyped actions or sequences of actions which are either re-enacted within an individual's lifetime or transmitted by repetition from multiple individuals.
This suggests that the configuration-algorithm responsible for the distinction between profitable vs. dangerous may be implemented by quite different neural networks. Experiments with artificial neuronal nets support this presumption.
Stereopsis in toads: Connecting ''what'' and ''where'' streams
Previously thought to be characteristic of solely primates and mammals with front-facing eyes, the ability to process depth information from multiple visual points in space has been determined to be possessed by most amphibians, namely, frogs and toads. From an evolutionary point of view, there has been substantial support for the idea that stereo vision has evolved as a natural progression for animals with binocular vision, meaning, a substantial distance between the two eyes. This theory would mean that stereopsis has evolved independently at least four times to account for stereo vision being present in mammals, birds, amphibians, and some invertebrates.For toads in particular, stereopsis would prove massively advantageous, as depth perception is particularly useful in calculating distance and aiding in catching prey.
In common toads, two visual information processing streams are involved in the recognition and localization of prey. The visual data is transmitted via tectofugal pathways that originate in the topographic map of the retinotectal system. The processing streams of both visual systems —one conveying information about the characteristics of the prey, the other about the current distance between the toad and the prey—are not completely separate from each other. Stereopsis and lens accommodation enable correspondence between the two.
Prey recognition uses calculations in retino-tectal and retino-pretecto-tectal/thalamic networks, the results of which are transmitted via tecto-bulbar/spinal projecting axons —ultimately to the hypoglossal nucleus, which triggers the motor coordination of snapping. The strategy of catching when determining the respective distance to the prey involves a tecto-tegmental relay circuit, which mainly uses monocular depth calculations. The information obtained from the accommodation of the eye lens makes it possible to estimate distances between the toad and its prey in a range between 5 and 20 cm, data that is also used to determine the absolute size of a prey object in order to ensure size constancy. Results from recording studies of toad's medullary neurons support the assumption that prey detection and local sign carrying tectal command elements converge on bulbar motor pattern generating nuclei.
As an equivalent of an innate releasing mechanism, it is proposed that a command releasing system for triggering prey capture includes visual command elements for prey 'recognition' AND visual command elements for prey 'localization', which control the 'orient' command:
• T5.2: recognized as prey AND T4 and T5.1: prey located in the peripheral
visual field ——> ORIENT !
• T5.2: recognized as prey AND T1.1 and T2.2: prey located in the frontal
visual field far afield ——> APPROACH !
• T5.2: recognized as prey AND T1.2: prey located binocularly at short distance ——>FIXATE !
• T5.2: recognized as prey AND T1.3 and T3: prey located binocularly in striking distance ——> SNAP !
Both processing streams in this multiple action system converge when the toad has its prey within striking distance. If the head end of an earthworm stretches in a way that is difficult to handle, the toad is prompted to tilt its head accordingly and choose a practical catching method, either by flicking its tongue or grabbing with its jaws. This binocular fixation process requires sensorimotor correspondence between configurative prey selection and object distance estimation. Since the experimental relaxation of the lens muscles with atropine had no significant effect on the accuracy of snapping in binocular toads —while one-eyed toads missed the target—it is assumed that stereopsis enables a finely tuned perception/action cycle during fixation.
The study on the interaction of spatial and spatio-temporal variations in contrast boundaries in the visual recognition of prey and threat objects raises the question of whether toads can distinguish and memorize visual details of moving stimuli. Yes, they do. Toads perceive different black-and-white patterns within the external dimensions of a configurative worm or bug shape. They demonstrate this through stimulus habituation, a type of non-associative learning. When a dummy prey of a pattern A circles around a toad in the direction of its longitudinal axis in a special experimental setup, the toad's successive orientation turning reactions to visually catch the prey decrease due to stimulus-specific habituation until A remaines unaddressed. But if, immediately after habituation to A, another prey dummy with a different pattern B triggers prey orienting, it can be concluded that the toad distinguished between A and B. If in the reverse type of experiment, the pattern A following habituation to B elicits no prey orienting, toads preferred B over A. If in both habituation series the second pattern dishabituates the prey-orienting activity to the same extent, both were discriminated and equally attractive to the toad.
Based on paired tests of different patterns, a hierarchical order in stimulus pattern specificity: the caudal dorsal thalamic structures, b) in pattern specific after-effects and memory: the ventral medial pallium, and c) in locus specificity with respect to areas of the visual field: the retino-tectal map.
Computer simulations demonstrate a remarkable match between the model performance and the original experimental data on which the ‚dishabituation hierarchy’ was based. A set of model predictions is presented, concerning mechanisms of habituation and cellular organization of the medial pallium, vMP. These studies serve as an example of a fruitful dialogue between experimentation and modeling, crucial for understanding brain functions. After vMP lesions, for example, stimulus habituation was abolished.
Stimulus specific habituation belongs to the evolutionary conserved neural circuits, from molluscs to mammals. The Aplysia gill and siphon withdrawal reflex of the marine snail Aplysia californica protects the gill and siphon from potentially threatening stimuli. To repeated release of this behavior with the same stimulus, the animal habituates in a stimulus-specific fashion in order to avoid wasted effort and be visually perceptive for new stimulus situations. Multidisciplinary experimental analyses of the complex molecular memory processes in sensori-motor integration of Aplysia result in the identification of a valuable model system with developments for medical application.