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 (neural basis of natural behavior). He began by observing the natural prey catching behavior of the common European toad (Bufo bufo).

Ewert’s work with 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 tectum and the thalamic-pretectal region, that were responsible for discriminating prey from non-prey and revealed the neural pathways that connected them. Furthermore, he found that the neural mechanisms are plastic and adaptable to varying environments and conditions.

Natural toad behavior

The common toad responds to a moving insect or worm prey with a series of stereotyped responses: (1) orienting toward prey, (2) stalking up to prey, (3) binocular fixation, (4) snapping, (5) swallowing and (6) mouth-wiping with fore limbs (Ewert 1974). This series of movement constitutes a stimulus-response chain, where each reaction of the toad serves as the subsequent stimulus for the next response. First, if a moving object catches the toad’s attention, the toad will orient towards the stimulus by turning its body to face it. Then it approaches the prey, focusing intently on it. During the attack, it snaps at the object with its tongue and swallows it. Finally, it wipes its mouth with a forelimb. These actions constitute a series of well-defined behavioral patterns.

One reason for this type of stimulus-response chain, is that unlike humans, toads do not have involuntary saccadic eye movements, so they cannot perform “tracking eye movements” (Ewert 1980). They must, therefore, depend on discriminating stimulus patterns that are either wholly or partially detected in their visual fields. As a result they have developed specific actions in response to a variety of visual stimuli that allow them to discriminate between edible prey and dangerous predators.

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. If it decides to orient towards the object, it commits itself to snapping. Even when the prey stimulus has been removed after binocular fixation, as long as the orienting behavior has been initiated, the toad will complete the entire sequence of responses.

Prey vs. predator response

When a toad is presented with a moving stimulus, it generally reacts with one of two responses. It will either engage in orienting (prey-catching) behavior or avoidance (escape) behavior, which consists of “planting-down” defensive postures or a crouching avoidance response.

In determining the 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.

In order to study the behavioral responses of toads to varying types of stimuli, Ewert conducted experiments by placing the toad in the center of a small cylindrical glass vessel. He then rotated a long strip of contrasting cardboard (acting as a visual ‘dummy’) around the vessel to mimic either prey or predator 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 stimuli that determine behavior.

Up to a certain size, squares rotated 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. In general, movement of a rectangle in the direction of its long axis is perceived by the toad to be wormlike, whereas movement along the short axis is interpreted as anti-wormlike.

It is important to note that stationary objects usually elicit no prey-catching or avoidance responses. In addition, the contrast between stimuli and background can significantly affect the type of behavior. White objects moving against a black background are usually more attractive as prey than black objects on white. However, this tendency is plastic and reverses seasonally, where black objects against a white background are much more effective at eliciting prey-catching behavior in the fall and winter (Ewert 1980).

Feature detectors and the visual system

In order to understand the neural mechanisms underlying the toad’s behavioral responses, Ewert performed a series of recording and stimulation experiments. First and foremost, the results allowed him to understand the way in which 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 stimuli.

First, the retina is connected to the optic tectum by three types of ganglion cells, each with an excitatory receptive field and a surrounding inhibitory receptive field, but differ in the diameter of their central excitatory receptive fields. Diameters in Class II ganglion cells are approximately four degrees. Those in Class III cells are about eight degrees and 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 particular part of its visual field, 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 thalamic-pretectal region (in the diencephalon) played significant roles in the analysis and interpretation of visual stimuli.

Stimulation experiments demonstrated that the tectum initiates orienting behavior. It contains two types of tectal neurons: Type I and Type II. Type I neurons are activated when the object in the toad’s visual field is extended in the direction of movement. Type II neurons fire less when the object is extended in a direction that is perpendicular to the direction of movement. Type I and II neurons, in combination, contribute to the ability of the tectum to initiate orienting behavior.

The thalamic-pretectal region, in contrast to the tectum, initiates avoidance behavior in the toad. More specifically, triggering the thalamic-pretectal region initiates a variety of protective movements such as eyelid closing, ducking and turning away (Ewert 1974). Four types of neurons in the region are responsible for the avoidance behavior and they are all sensitive to different types of stimuli. The first is activated by objects that are extended perpendicularly to the direction of motion. The second is activated by movement of an object toward the toad. The third is activated by large stationary objects and the fourth is activated by stimulation of the balance sensors in the toad’s ear. Stimulation of (any combination of) these four types of neurons would cause the toad to display protective behaviors.

Furthermore lesioning experiments led to the discovery of pathways extending between the tectum and the thalamic-pretectal region. When the tectum was removed, orienting behavior disappeared, and when the thalamic-pretectal region was removed, avoidance behavior was entirely absent while orienting behavior was much more enhanced even in the presence of predator stimuli (Zupanc 2004). Finally, when one half of the thalamic-pretectal region was removed, the disinhibition applied to the entire visual field of the opposite side. These experiments demonstrated the inhibitory pathways that extended from the thalamus to the tectum.

ee also

* Jörg-Peter Ewert
* Toad

References

* Carew, T.J (2000). Feature analysis in Toads. In "Behavioral Neurobiology", Sunderland, MA: Sinauer, 95-119.
* Ewert, J.-P. (1974). The neural basis of visually guided behavior. "Scientific American", 230(3), 34-42.
* Ewert, J.-P. (1980). "Neuroethology: an introduction to the neurophysiological fundamentals of behavior". Springer-Verlag, Berlin/Heidelberg/New York.
* Zupanc, G. (2004) Behavioral Neurobiology: An Integrative Approach. Oxford University Press. 121-132.