Jamming avoidance response In 1963, Akira Watanabe and Kimihisa Takeda discovered the behavior of the
jamming avoidance response in the knifefish
Eigenmannia sp. In collaboration with T.H. Bullock and colleagues, the behavior was further developed. Finally, the work of
W. Heiligenberg expanded it into a full neuroethology study by examining the series of neural connections that led to the behavior.
Eigenmannia is a weakly electric fish that can generate electric discharges through electrocytes in its tail. Furthermore, it has the ability to electrolocate by analyzing the perturbations in its electric field. However, when the frequency of a neighboring fish's current is very close (less than 20 Hz difference) to that of its own, the fish will avoid having their signals interfere through a behavior known as Jamming Avoidance Response. If the neighbor's frequency is higher than the fish's discharge frequency, the fish will lower its frequency, and vice versa. The sign of the frequency difference is determined by analyzing the "beat" pattern of the incoming interference which consists of the combination of the two fish's discharge patterns. Neuroethologists performed several experiments under
Eigenmannias natural conditions to study how it determined the sign of the frequency difference. They manipulated the fish's discharge by injecting it with curare which prevented its natural electric organ from discharging. Then, an electrode was placed in its mouth and another was placed at the tip of its tail. Likewise, the neighboring fish's electric field was mimicked using another set of electrodes. This experiment allowed neuroethologists to manipulate different discharge frequencies and observe the fish's behavior. From the results, they were able to conclude that the electric field frequency, rather than an internal frequency measure, was used as a reference. This experiment is significant in that not only does it reveal a crucial neural mechanism underlying the behavior but also demonstrates the value neuroethologists place on studying animals in their natural habitats.
Feature analysis in toad vision The recognition of prey and predators in the toad was first studied in depth by
Jörg-Peter Ewert (Ewert 1974, 2004; see also Carew 2000, Zupanc 2004). In the early 1960s, he began by observing the natural prey-catching behavior of the common toad (
Bufo bufo) and concluded that the animal followed a sequence that consisted of orientational head and body turning, stalking, binocular fixation and snapping at a small visual object, while a large object was avoided. Asking either teleologically about the purpose of a behavioral action or asking causal-analytically about the processes that allow the animal to recognize appropriate stimuli before deciding on an action, he opted for the latter, which is of interest to neuroethological multi-method research. With the aid of motor driven perimetric procedures he moved bars of different configurations as dummies and determined what 'small' or 'large' means in terms of invariant stimulus features for the toad's recognition of prey or threat. It was observed that the worm configuration, which signaled prey, was initiated by movement along the object's long axis, whereas anti-worm configuration, which signaled threat or predator, was due to movement along the short axis. This observation was decisive for the configurative experimental paradigm: when a two-dimensional visual object moves, it is determined by its extension (e) parallel to the direction of movement (ep) and its extension transverse to the direction of movement (et). Toads interpret the extension of ep as prey-like (providing ep lies within behaviorally relevant limits and et is sufficiently small), while they interpret the extension of et as threatening. The distinction between ep- and et-features in relation to the 'worm' vs. 'anti-worm' configuration is independent (invariant) of changes in other stimulus parameters such as color, contrast of the stimulus background, the motion vector in relation to the direction in which the object moves in the toad's field of view on the x, y, or z axis, and, within behaviorally relevant limits, also independent of object size and speed. The use of experimental variations of ep and et enables a quantitative description of
sign stimuli according to Tinbergen's concept of
gestalt perception from a behavioral science and neurophysiological perspective. This means that the previous classification of toads' prey and predators into size categories of 'small' and 'large' objects, based solely on surface area, is insufficient. For instance, a small black bar measuring 2.5 mm x 10 mm or a large black bar measuring 2.5 mm x 80 mm, moving in a worm configuration against a white background, released intense prey-catching activity. Conversely, the same small or large bars in anti-worm configuration signaled a threat. Ewert and his colleagues adopted a variety of methods to study the behaviors of toads to prey and predators, as well as behavior-correlated mapping of brain activity using the 14C-2DG method. File: 14C2DG.png|thumb|Dorsal view (A) of the toad’s brain and eyes. B) Different visual configurational stimuli (S) release different behavior-correlated [14C]-2DG-uptake (color code: increasing from blue to red/black). RF, receptive field of a retinal (R) ganglion cell (G) projecting via optic nerve (ON) to the contralateral brain side: caudal thalamic pretectal region (TH) and optic tectum (T). DT, dorsal tectum; VT, ventral tectum; MP, posterior ventral medial pallium. M, medulla oblongata. The color-coded brain transverse sections at different levels a-d show increases in [14C]-2DG-uptake: (a) unilaterally in MP to a contralaterally moving prey capture releasing large square after conditioning by hand feeding, (b) in TH and DT to a threatening large square, (c) in TH to a threatening antiworm-like bar, and (d) in VT to a snapping releasing worm-like bar. Combined after Finkenstädt 1985 and Ewert 2022. They also conducted recording experiments where they inserted electrodes into the brain, while the toad was presented with worm-like or anti-worm-like stimuli or square objects of variable edge length. This technique was repeated at different levels of the visual system and also allowed
feature detectors to be identified. It was shown that the stimulus features ep and et are processed in the contralateral retino-topic maps of the retina: ep preferably in the optic tectum and et preferably in the pretectal thalamus. In focus was the discovery of prey-selective neurons of the Type T5.2 in the optic tectum, whose axons could be traced along the tecto-bulbar tract towards the snapping pattern generating cells in the hypoglossal nucleus. The neurophysiological evidence for the tecto-bulbar projection of a T5.2 neuron was verified by antidromic electrical stimulation and three tests: (i) constant latency, (ii) following ability to high frequency stimulation, and (iii) spike collision. In test (iii), a visually elicited orthodromically traveling spike — recorded from the T5.2-cell's axon — triggered an antidromically propagating spike in response to focal electrical stimulation of the tecto-bulbar tract at the level of the hypoglossal nucleus. When both spikes met along the same axon, they annihilated each other. The discharge patterns of T5.2 prey-selective tectal neurons in response to prey objects – recorded in freely moving toads – 'predicted' prey-catching reactions such as snapping. Another approach, called stimulation experiment, was also carried out in freely moving toads. Focal electrical stimuli were applied to different regions of the brain, and the toad's response was observed. When the pretectal thalamic region was stimulated, the toad exhibited escape responses, but when the optic tectum was stimulated in an area close to prey-selective neurons, the toad engaged in prey catching behavior (Carew 2000). Furthermore, neuroanatomical experiments were carried out where the toad's pretectal thalamic connection to the ipsilateral optic tectum was lesioned and the resulting deficit noted: the prey-selective properties were abolished both in the responses of prey-selective neurons and in the prey catching behavior. These and other experiments suggest that prey selectivity results from thalamic pretectal inhibitory influences to the optic tectum. It is suggested that thalamic TH4 neurons, projecting their axons in the bulbar/spinal tract, process both excitatory pretectal thalamic influences from feature et and excitatory tectal influences from feature ep in order to trigger predator avoidance behaviors. With regard to the releasing mechanisms of the prey capture sequence it is suggested that the release of each action - orienting, stalking, fixating or snapping - requires prey recognition and that the type of action in the sequence is determined by the localization of the prey in space. For example, a toad's prey capture release mechanism for orienting toward prey involves visual command elements for prey recognition (
prey feature detecting neurons T5.2) AND visual command elements for prey localization (
local sign detecting neurons T5.1 and T4). Ewert and coworkers showed in toads that there are stimulus-response mediating pathways that translate perception (of visual sign stimuli) into action (adequate behavioral responses). In addition there are modulatory loops that initiate, modify or specify this mediation (Ewert 2004). Regarding the latter, for example, the telencephalic caudal ventral striatum is involved in a loop gating the stimulus-response mediation in a manner of directed attention. The posterior telencephalic ventral medial pallium („primordium hippocampi"), however, is involved in loops that either modify prey-selection due to associative learning or specify prey-selection due to stimulus-selective habituation, respectively. ==Computational neuroethology==