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 Bioelectrogenesis, generate electric fields, whether to sense things around them, for defence, or to stun prey. Most fish able to produce shocks are also electroreceptive, meaning that they can sense electric ...

. 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. Frequency is an important parameter used in science and engineering to specify the rate of oscillatory and vibratory phenomena, such as mechanical vibrations, audio ...

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, such ...

. 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 considerably smaller portion in the Northern Hemisphere. It can also be described as the southern Subregion#Americas, subregion o ...

n species ''

Eigenmannia virescens ''Eigenmannia virescens'', the glass knifefish, is a weakly electric freshwater fish found across South America. It is marketed as an aquarium fish. Description The appendix on the body has black lines running through the bottom of the sides, ...

''. 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 (the ...

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 and ...

'', as well as in the

Africa Africa is the world's second-largest and second-most populous continent after Asia. At about 30.3 million km2 (11.7 million square miles) including adjacent islands, it covers 20% of Earth's land area and 6% of its total surfac ...

n species ''

Gymnarchus niloticus The African knifefish, ''Gymnarchus niloticus'' – also called the ''aba aba'' – is an electric fish, living at the bottoms of rivers and lakes. It is the only species in the genus ''Gymnarchus'' and the family Gymnarchidae, within the or ...

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

vertebrate Vertebrates () are animals with a vertebral column (backbone or spine), and a cranium, or skull. The vertebral column surrounds and protects the spinal cord, while the cranium protects the brain. The vertebrates make up the subphylum Vertebra ...

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 s ...

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 Elect ...

'', which has a quasi-

sinusoidal A sine wave, sinusoidal wave, or sinusoid (symbol: ∿) is a periodic wave whose waveform (shape) is the trigonometric sine function. In mechanics, as a linear motion over time, this is '' simple harmonic motion''; as rotation, it correspond ...

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 a gas). In electrochemical cells, electrodes are essential parts that can consist of a varie ...

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 Theodore Holmes Bullock (16 May 1915 – 20 December 2005) is one of the founding fathers of neuroethology. During a career spanning nearly seven decades, this American academic was esteemed both as a pioneering and influential neuroscientist, ex ...

, Robert Hamstra Jr., and Henning Scheich. Gymnarchus niloticus005

In 1975,

Walter Heiligenberg Walter F. Heiligenberg (January 31, 1938 – September 8, 1994) was a German American scientist best known for his neuroethology work on one of the best neurologically understood behavioral patterns in a vertebrate, ''Eigenmannia''. This weakly el ...

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 comm ...

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 develop ...

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 ( or ; or ) 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 America for hunting and for therapeutic purposes, curare only ...

, 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 A model is an informative representation of an object, person, or system. The term originally denoted the plans of a building in late 16th-century English, and derived via French and Italian ultimately from Latin , . Models can be divided into ...

Sensory coding

When the stimulus frequency and discharge frequency are close to each other, the two amplitude-time waves undergo

interference Interference is the act of interfering, invading, or poaching. Interference may also refer to: Communications * Interference (communication), anything which alters, modifies, or disrupts a message * Adjacent-channel interference, caused by extra ...

, and the electroreceptive organs perceive a single wave with an intermediate frequency. In addition, the combined stimulus-EOD wave has a beat pattern, 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, such ...

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 (American English), neurone (British English), or nerve cell, is an membrane potential#Cell excitability, excitable cell (biology), cell that fires electric signals called action potentials across a neural network (biology), neural net ...

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 The midbrain or mesencephalon is the uppermost portion of the brainstem connecting the diencephalon and cerebrum with the pons. It consists of the cerebral peduncles, tegmentum, and tectum. It is functionally associated with vision, hearing, mo ...

. 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 In the human brain, 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 t ...

, 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: * A socio-political or established or existing order, e.g. World order, Ancien Regime, Pax Britannica * Categorization, the process in which ideas and objects are recognized, differentiated, and understood * H ...

of weakly electric fish,

from

and

Osteoglossiformes Osteoglossiformes , meaning "bony tongues" in Ancient Greek, 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 ...

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, such ...

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 (; : genera ) is a taxonomic rank above species and below family as used in the biological classification of living and fossil organisms as well as viruses. In binomial nomenclature, the genus name forms the first part of the binomial s ...

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 In biology, a clade (), also known as a Monophyly, monophyletic group or natural group, is a group of organisms that is composed of a common ancestor and all of its descendants. Clades are the fundamental unit of cladistics, a modern approach t ...

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".