Jamming avoidance response in glass knifefish

The jamming avoidance response is a behavior of some species of

weakly electric fish An electric fish is any fish that can generate electric fields. Most electric fish are also electroreceptive, meaning that they can sense electric fields. The only exception is the stargazer family. Electric fish, although a small minority, in ...

. It occurs when two electric fish with wave discharges meet – if their discharge

frequencies Frequency is the number of occurrences of a repeating event per unit of time. It is also occasionally referred to as ''temporal frequency'' for clarity, and is distinct from ''angular frequency''. Frequency is measured in hertz (Hz) which is e ...

are very similar, each fish shifts its discharge frequency to increase the difference between the two. By doing this, both fish prevent jamming of their sense of

electroreception Electroreception and electrogenesis are the closely-related biological abilities to perceive electrical stimuli and to generate electric fields. Both are used to locate prey; stronger electric discharges are used in a few groups of fishes to st ...

. The behavior has been most intensively studied in the

South America South America is a continent entirely in the Western Hemisphere and mostly in the Southern Hemisphere, with a relatively small portion in the Northern Hemisphere at the northern tip of the continent. It can also be described as the sou ...

n species '' Eigenmannia virescens''. It is also present in other

Gymnotiformes The Gymnotiformes are an order of teleost bony fishes commonly known as Neotropical knifefish or South American knifefish. They have long bodies and swim using undulations of their elongated anal fin. Found almost exclusively in fresh water (t ...

such as ''

Apteronotus ''Apteronotus'' is a genus of weakly electric knifefish in the family Apteronotidae, distinguished by the presence of a tiny tail fin. This genus is restricted to tropical and subtropical South America (Amazon, Orinoco, Río de la Plata an ...

'', as well as in the

Africa Africa is the world's second-largest and second-most populous continent, after Asia in both cases. At about 30.3 million km2 (11.7 million square miles) including adjacent islands, it covers 6% of Earth's total surface area ...

n species ''

Gymnarchus niloticus ''Gymnarchus niloticus'' – commonly known as the ''aba'', ''aba aba'', frankfish, freshwater rat-tail, ''poisson-cheval'', or African knifefish – is an electric fish, and the only species in the genus ''Gymnarchus'' and the family Gymnarchida ...

''. The jamming avoidance response was one of the first complex behavioral responses in a

vertebrate Vertebrates () comprise all animal taxa within the subphylum Vertebrata () ( chordates with backbones), including all mammals, birds, reptiles, amphibians, and fish. Vertebrates represent the overwhelming majority of the phylum Chordata, with ...

to have its neural circuitry completely specified. As such, it holds special significance in the field of

neuroethology Neuroethology is the evolutionary and comparative approach to the study of animal behavior and its underlying mechanistic control by the nervous system. It is an interdisciplinary science that combines both neuroscience (study of the nervous syste ...

Discovery

The jamming avoidance response (JAR) was discovered by Akira Watanabe and Kimihisa Takeda in 1963. The fish they used was an unspecified species of ''

Eigenmannia ''Eigenmannia'' is a genus of fish in the family Sternopygidae (glass knifefishes) native to tropical and subtropical South America (south to the Río de la Plata Basin), and Panama.Peixoto, L.A.W., Dutra, G.M. & Wosiacki, W.B. (2015). The Elec ...

'', which has a quasi-

sinusoidal A sine wave, sinusoidal wave, or just sinusoid is a mathematical curve defined in terms of the '' sine'' trigonometric function, of which it is the graph. It is a type of continuous wave and also a smooth periodic function. It occurs often i ...

wave discharge of about 300 Hz. They found that when a sinusoidal electrical stimulus is emitted from an

electrode An electrode is an electrical conductor used to make contact with a nonmetallic part of a circuit (e.g. a semiconductor, an electrolyte, a vacuum or air). Electrodes are essential parts of batteries that can consist of a variety of materials ...

near the fish, if the stimulus frequency is within 5 Hz of the fish's electric organ discharge (EOD) frequency, the fish alters its EOD frequency to increase the difference between its own frequency and the stimulus frequency. Stimuli above the fish's EOD frequency push the EOD frequency downwards, while frequencies below that of the fish push the EOD frequency upwards, with a maximum change of about ±6.5 Hz. This behavior was given the name "jamming avoidance response" several years later in 1972, in a paper by Theodore Bullock, Robert Hamstra Jr., and Henning Scheich. Gymnarchus niloticus005

In 1975, Walter Heiligenberg discovered a JAR in the distantly-related ''

'', the African knifefish, showing that the behavior had

convergently evolved Convergent evolution is the independent evolution of similar features in species of different periods or epochs in time. Convergent evolution creates analogous structures that have similar form or function but were not present in the last com ...

in two separate lineages.

Behavior

''Eigenmannia'' and other weakly electric fish use active electrolocation – they can locate objects by generating an electric field and detecting distortions in the field caused by interference from those objects. Electric fish use their

electric organ An electric organ, also known as electronic organ, is an electronic keyboard instrument which was derived from the harmonium, pipe organ and theatre organ. Originally designed to imitate their sound, or orchestral sounds, it has since develope ...

to create electric fields, and they detect small distortions of these fields using special electroreceptive organs in the skin. All fish with the JAR are wave-discharging fish that emit steady quasi-sinusoidal discharges. For the genus ''Eigenmannia'', frequencies range from 240 to 600 Hz. The EOD frequency is very steady, typically with less than 0.3% variation over a 10-minute time span. If a neighboring sinusoidal electric field is discharging close to the fish's EOD frequency, it causes interference which results in sensory confusion in the fish and sufficient jamming to prevent it from electrolocating effectively. ''Eigenmannia'' typically are within the electric field range of three to five other fish of the same species at any time. If many fish are located near each other, it is beneficial for each fish to distinguish between their own signal and those of others; this can be done by increasing the frequency difference between their discharges. Therefore, it seems to be the function of the JAR to avoid sensory confusion among neighboring fish. To determine how close the stimulus frequency is to the discharge frequency, the fish compares the two frequencies using its electroreceptive organs, rather than comparing the discharge frequency to an internal pacemaker; in other words, the JAR relies only on sensory information. This was determined experimentally by silencing a fish's electric organ with

curare Curare ( /kʊˈrɑːri/ or /kjʊˈrɑːri/; ''koo-rah-ree'' or ''kyoo-rah-ree'') is a common name for various alkaloid arrow poisons originating from plant extracts. Used as a paralyzing agent by indigenous peoples in Central and South ...

, and then stimulating the fish with two external frequencies. The JAR, measured from the electromotor neurons in the spinal cord, depended only on the frequencies of the external stimuli, and not on the frequency of the pacemaker.

Neurobiology

Pathway in ''Eigenmannia'' (Gymnotiformes)

Most of the JAR pathway in the South American Gymnotiformes has been worked out using ''Eigenmannia virescens'' as a model system.

Sensory coding

When the stimulus frequency and discharge frequency are close to each other, the two amplitude-time waves undergo interference, and the electroreceptive organs perceive a single wave with an intermediate frequency. In addition, the combined stimulus-EOD wave has a

beat pattern Conducting is the art of directing a musical performance, such as an orchestral or choral concert. It has been defined as "the art of directing the simultaneous performance of several players or singers by the use of gesture." The primary duties ...

, with the beat frequency equal to the frequency difference between the stimulus and EOD. Gymnotiforms have two classes of electroreceptive organs, the

ampullary receptor Electroreception and electrogenesis are the closely-related biological abilities to perceive electrical stimuli and to generate electric fields. Both are used to locate prey; stronger electric discharges are used in a few groups of fishes to stu ...

s and the tuberous receptors. Ampullary receptors respond to low-frequency stimulation less than 40 Hz and their role in the JAR is currently unknown. Tuberous receptors respond to higher frequencies, firing best near the fish's normal EOD frequency. Tuberous receptors themselves have two types, the T-unit and P-unit. The T-unit (T standing for time, meaning phase in the cycle) fires synchronously with the signal frequency by firing a spike on every cycle of the waveform. P-units (P standing for probability) tend to fire when the amplitude increases and fire less when it decreases. Under conditions of jamming, the P-unit fires on the amplitude peaks of the beat cycle where the two waves constructively interfere. So, a combined stimulus-EOD signal causes T-units to fire at the intermediate frequency, and causes P-unit firing to increase and decrease periodically with the beat.

Processing in the brain

The time-coding T-units converge onto

neurons A neuron, neurone, or nerve cell is an electrically excitable cell that communicates with other cells via specialized connections called synapses. The neuron is the main component of nervous tissue in all animals except sponges and placozoa ...

called spherical cells in the electrosensory lateral line lobe. By combining information from multiple T-units, the spherical cell is even more precise in its time coding. Amplitude-coding P-units converge onto pyramidal cells, also in the electrosensory lateral line lobe. Two types of pyramidal cells exist: excitatory E-units, which fire more when stimulated by P-units, and inhibitory I-units, which fire less when stimulated by inhibitory interneurons activated by P-units. Spherical cells and pyramidal cells then project to the torus semicircularis, a structure with many laminae (layers) in the mesencephalon. Phase and amplitude information are integrated here to determine whether the stimulus frequency is greater or less than the EOD frequency. Sign-selective neurons in the deeper layers of the torus semicircularis are selective to whether the frequency difference is positive or negative; any given sign-selective cell fires in one case but not in the other.

Output

Sign-selective cells input into the nucleus electrosensorius in the

diencephalon The diencephalon (or interbrain) is a division of the forebrain (embryonic ''prosencephalon''). It is situated between the telencephalon and the midbrain (embryonic ''mesencephalon''). The diencephalon has also been known as the 'tweenbrain in o ...

, which then projects onto two different pathways. Neurons selective for a positive difference (stimulus greater than EOD) stimulate the prepacemaker nucleus, while neurons selective for a negative difference (stimulus less than EOD) inhibit the sublemniscal prepacemaker nucleus. Both prepacemaker nuclei send projections to the pacemaker nucleus, which ultimately controls the frequency of the EOD.

Pathway in ''Gymnarchus'' (Osteoglossiformes)

The neural pathway of JAR in ''Gymnarchus'' is nearly identical to that of the Gymnotiformes, with a few minor differences. S-units in ''Gymnarchus'' are time coders, like the T-units in Gymnotiformes. O-units code the signal's intensity, like P-units in Gymnotiformes, but respond over a narrower range of intensities. In ''Gymnarchus'', phase differences between EOD and stimulus are calculated in the electrosensory lateral line lobe rather than in the torus semicircularis.

Phylogeny and evolution of weakly electric fish

There are two main

orders Order, ORDER or Orders may refer to: * Categorization, the process in which ideas and objects are recognized, differentiated, and understood * Heterarchy, a system of organization wherein the elements have the potential to be ranked a number of ...

of weakly electric fish,

from

and

Osteoglossiformes Osteoglossiformes (Greek: "bony tongues") is a relatively primitive order of ray-finned fish that contains two sub-orders, the Osteoglossoidei and the Notopteroidei. All of at least 245 living species inhabit freshwater. They are found in South ...

from

Electroreception Electroreception and electrogenesis are the closely-related biological abilities to perceive electrical stimuli and to generate electric fields. Both are used to locate prey; stronger electric discharges are used in a few groups of fishes to st ...

most likely arose independently in the two lineages. Weakly electric fish are mostly pulse-dischargers, which do not perform the JAR, while some are wave-dischargers. Wave-discharge evolved in two taxa: the superfamily Apteronotoidea (order

), and the species ''

'' (order

). Notable

genera Genus ( plural genera ) is a taxonomic rank used in the biological classification of living and fossil organisms as well as viruses. In the hierarchy of biological classification, genus comes above species and below family. In binomial nomenclat ...

in Apteronotoidea that perform JAR include ''

'' and ''

''. Though they evolved the JAR separately, the South American and African taxa (boldface in the tree) have

nearly identical neural computational mechanisms and behavioral responses to avoid jamming, with only minor differences. The phylogeny of the weakly electric fish

clade A clade (), also known as a monophyletic group or natural group, is a group of organisms that are monophyletic – that is, composed of a common ancestor and all its lineal descendants – on a phylogenetic tree. Rather than the English ter ...

s, omitting non-electric and strongly-electric fishes, shows major events in their evolution. In the tree, "sp" means "a species" and "spp" means "multiple species".