Jamming avoidance response
Encyclopedia
The jamming avoidance response or JAR is a behavior performed by some species of weakly electric fish. The JAR occurs when two electric fish with wave discharges meet – if their discharge frequencies
are very similar, each fish will shift its discharge frequency to increase the difference between the two fish's discharge frequencies. By doing this, both fish prevent jamming of their sense of electroreception
.
The behavior has been most intensively studied in the South America
n species Eigenmannia virescens
(order Gymnotiformes
). The behavior is also present in other Gymnotiformes such as Apteronotus
, as well as in the Africa
n species Gymnarchus niloticus
(order Osteoglossiformes
). The JAR was one of the first complex behavioral responses in a vertebrate
to have its neural circuitry completely specified. As such, the JAR holds special significance in the field of neuroethology
.
. The fish they used was an unspecified species of Eigenmannia
, which has a quasi-sinusoidal
wave-like discharge of about 300 Hz
. They found that when a sinusoidal electrical stimulus is emitted from an electrode
near the fish, if the stimulus frequency is within 5 Hz of the fish's electric organ discharge (EOD) frequency, the fish will alter its EOD frequency to increase the difference between its own frequency and the stimulus frequency. Stimuli above the fish's EOD frequency will "push" the EOD frequency downwards, while frequencies below the that of the fish will push the EOD frequency upward, 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.
The JAR was discovered in the distantly-related Gymnarchus niloticus
by Walter Heiligenberg
in 1975 , showing that the behavior had convergently evolved
in two separate lineages.
and other weakly electric fish all use active electrolocation – they can locate objects by generating an electric field and detecting distortions in the field caused by interference from the object. Electric fish use the electric organ
to create electric fields, and they detect fields using special electroreceptive organs in the skin.
All fish that perform 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 electric field is discharging sinusoidally close to the fish's EOD frequency, then it will cause sensory confusion in the fish, jamming it and preventing it from electrolocating effectively. Eigenmannia typically are within the electric field range of three to five conspecifics at any time . If many fish are located near each other, it would be 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 that 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
, and then stimulating the fish with two external frequencies. The JAR response, 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.
.
, with the beat frequency equal to the frequency difference between stimulus and EOD.
Gymnotiforms have two classes of electroreceptive organs, the ampullary receptors and the tuberous receptor
s. Ampullary receptors respond to low-frequency stimulation less than 40 Hz and are not involved in the JAR. 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 fires synchronously with the signal frequency, by firing a spike on every cycle of the waveform. P-units 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 will cause T-units to fire at the intermediate frequency, and cause P-unit firing to increase and decrease periodically with the beat.
Spherical cells and pyramidal cells then project to the torus semicircularis (TS), a structure with many laminae, or layers. The TS is located 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 TS are selective to whether the frequency difference is positive or negative; any given sign-selective cell will fire in one case but not for the other.
, which then projects onto two different pathways. Neurons selective for a positive difference (stimulus > EOD) stimulate the prepacemaker nucleus (PPn-G), while neurons selective for a negative difference (stimulus < EOD) inhibit the sublemniscal prepacemaker nucleus (sPPn). These prepacemaker nuclei, PPn-G and sPPn, send projections to the pacemaker nucleus (Pn), which ultimately controls the frequency of the EOD.
In Gymnarchus, phase differences between EOD and stimulus are calculated in the electrosensory lateral line lobe (ELL) rather than in the torus semicircularis (TS).
of weakly electric fish, Gymnotiformes
from South America
and Osteoglossiformes
from Africa
. Electroreception
most likely arose independently in the two lineages. Weakly electric fish are either pulse-dischargers or wave-dischargers; most are pulse-dischargers, which do not perform the JAR. Wave-discharge evolved in two taxa: 1) the superfamily Apteronotoidea (order Gymnotiformes
), and 2) the species Gymnarchus niloticus
(order Osteoglossiformes
). Notable genera
in Apteronotoidea that perform JAR include Eigenmannia
and Apteronotus
.
Though they evolved the JAR separately, the South American and African taxa have convergently evolved
nearly identical neural computational mechanisms and behavioral responses to avoid jamming, with only minor differences.
Frequency
Frequency is the number of occurrences of a repeating event per unit time. It is also referred to as temporal frequency.The period is the duration of one cycle in a repeating event, so the period is the reciprocal of the frequency...
are very similar, each fish will shift its discharge frequency to increase the difference between the two fish's discharge frequencies. By doing this, both fish prevent jamming of their sense of electroreception
Electroreception
Electroreception is the biological ability to perceive natural electrical stimuli. It has been observed only in aquatic or amphibious animals, since water is a much better conductor than air. Electroreception is used in electrolocation and for electrocommunication.- Overview :Electroreception is...
.
The behavior has been most intensively studied in the South America
South America
South America is a continent situated in the Western Hemisphere, mostly in the Southern Hemisphere, with a relatively small portion in the Northern Hemisphere. The continent is also considered a subcontinent of the Americas. It is bordered on the west by the Pacific Ocean and on the north and east...
n species Eigenmannia virescens
Glass knifefish
Glass knifefishes are fishes in the family Sternopygidae in the order Gymnotiformes. Species are also known as rattail knifefishes.These fishes inhabit freshwater streams and rivers in Panama and South America...
(order Gymnotiformes
Gymnotiformes
The Gymnotiformes are a group of teleost bony fishes commonly known as the Neotropical or South American knifefishes. They have long bodies and swim using undulations of their elongated anal fin...
). The behavior is also present in other Gymnotiformes such as Apteronotus
Apteronotus
Apteronotus is a genus of weakly electric knifefish in the family Apteronotidae, distinguished by the presence of a tiny caudal fin.-Species:* Black ghost knifefish, Apteronotus albifrons ....
, as well as in the Africa
Africa
Africa is the world's second largest and second most populous continent, after Asia. At about 30.2 million km² including adjacent islands, it covers 6% of the Earth's total surface area and 20.4% of the total land area...
n species Gymnarchus niloticus
Gymnarchus niloticus
Gymnarchus niloticus – commonly known as the aba, aba aba, frankfish, freshwater rat-tail or African knifefish – is an electric fish, and the only species in the genus Gymnarchus and the family Gymnarchidae within the order Osteoglossiformes...
(order Osteoglossiformes
Osteoglossiformes
Osteoglossiformes is a relatively primitive order of ray-finned fish that contains two sub-orders, the Osteoglossoidei and the Notopteroidei. All of the living species inhabit freshwater...
). The JAR was one of the first complex behavioral responses in a vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
to have its neural circuitry completely specified. As such, the JAR holds special significance in the field of neuroethology
Neuroethology
Neuroethology is the evolutionary and comparative approach to the study of animal behavior and its underlying mechanistic control by the nervous system...
.
Discovery
The jamming avoidance response was discovered by Akira Watanabe and Kimihisa Takeda in 1963 while working at the Tokyo Medical and Dental UniversityTokyo Medical and Dental University
is part of Japan's national university system. Tokyo Medical and Dental University offers baccalaureate and graduate degrees in medicine, dentistry, and related fields.- History :...
. The fish they used was an unspecified species of Eigenmannia
Glass knifefish
Glass knifefishes are fishes in the family Sternopygidae in the order Gymnotiformes. Species are also known as rattail knifefishes.These fishes inhabit freshwater streams and rivers in Panama and South America...
, which has a quasi-sinusoidal
Sine wave
The sine wave or sinusoid is a mathematical function that describes a smooth repetitive oscillation. It occurs often in pure mathematics, as well as physics, signal processing, electrical engineering and many other fields...
wave-like discharge of about 300 Hz
Hertz
The hertz is the SI unit of frequency defined as the number of cycles per second of a periodic phenomenon. One of its most common uses is the description of the sine wave, particularly those used in radio and audio applications....
. They found that when a sinusoidal electrical stimulus is emitted from an electrode
Electrode
An electrode is an electrical conductor used to make contact with a nonmetallic part of a circuit...
near the fish, if the stimulus frequency is within 5 Hz of the fish's electric organ discharge (EOD) frequency, the fish will alter its EOD frequency to increase the difference between its own frequency and the stimulus frequency. Stimuli above the fish's EOD frequency will "push" the EOD frequency downwards, while frequencies below the that of the fish will push the EOD frequency upward, 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.
The JAR was discovered in the distantly-related Gymnarchus niloticus
Gymnarchus niloticus
Gymnarchus niloticus – commonly known as the aba, aba aba, frankfish, freshwater rat-tail or African knifefish – is an electric fish, and the only species in the genus Gymnarchus and the family Gymnarchidae within the order Osteoglossiformes...
by Walter Heiligenberg
Walter Heiligenberg
Walter Heiligenberg is best known for his contribution to neuroethology through his work on one of the best neurologically understood behavioral patterns in vertebrate, Eigenmannia...
in 1975 , showing that the behavior had convergently evolved
Convergent evolution
Convergent evolution describes the acquisition of the same biological trait in unrelated lineages.The wing is a classic example of convergent evolution in action. Although their last common ancestor did not have wings, both birds and bats do, and are capable of powered flight. The wings are...
in two separate lineages.
Behavior
EigenmanniaGlass knifefish
Glass knifefishes are fishes in the family Sternopygidae in the order Gymnotiformes. Species are also known as rattail knifefishes.These fishes inhabit freshwater streams and rivers in Panama and South America...
and other weakly electric fish all use active electrolocation – they can locate objects by generating an electric field and detecting distortions in the field caused by interference from the object. Electric fish use the electric organ
Electric organ
In biology, the electric organ is an organ common to all electric fish used for the purposes of creating an electric field. The electric organ is derived from modified nerve or muscle tissue...
to create electric fields, and they detect fields using special electroreceptive organs in the skin.
All fish that perform 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 electric field is discharging sinusoidally close to the fish's EOD frequency, then it will cause sensory confusion in the fish, jamming it and preventing it from electrolocating effectively. Eigenmannia typically are within the electric field range of three to five conspecifics at any time . If many fish are located near each other, it would be 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 that 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
Curare is a common name for various arrow poisons originating from South America. The three main types of curare are:* tubocurare...
, and then stimulating the fish with two external frequencies. The JAR response, 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.
Pathway in Gymnotiformes
Most of the JAR pathway in the South American Gymnotiformes has been worked out using Eigenmannia virescens as a model systemModel organism
A model organism is a non-human species that is extensively studied to understand particular biological phenomena, with the expectation that discoveries made in the organism model will provide insight into the workings of other organisms. Model organisms are in vivo models and are widely used to...
.
Sensory Coding
When the stimulus frequency and discharge frequency are close to each other, the two amplitude-time waves will undergo interference, and the electroreceptive organs will perceive a single wave with an intermediate frequency. In addition, the combined stimulus-EOD wave will have a beat patternBeat (acoustics)
In acoustics, a beat is an interference between two sounds of slightly different frequencies, perceived as periodic variations in volume whose rate is the difference between the two frequencies....
, with the beat frequency equal to the frequency difference between stimulus and EOD.
Gymnotiforms have two classes of electroreceptive organs, the ampullary receptors and the tuberous receptor
Tuberous receptor
Tuberous receptors are electroreceptors that are specialized to respond to high-frequency electrical fields , and hence are found only in fish with an active electrical sense that can generate their own electrical fields. They are mostly found on weakly electric fishes such as gymnotiforms and...
s. Ampullary receptors respond to low-frequency stimulation less than 40 Hz and are not involved in the JAR. 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 fires synchronously with the signal frequency, by firing a spike on every cycle of the waveform. P-units 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 will cause T-units to fire at the intermediate frequency, and cause P-unit firing to increase and decrease periodically with the beat.
Processing in the Brain
The time-coding T-units converge onto neurons called spherical cells in the electrosensory lateral line lobe (ELL). 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 ELL. Two types of pyramidal cells exist: 1) excitatory E-units, which fire more when stimulated by P-units, and 2) 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 (TS), a structure with many laminae, or layers. The TS is located in the mesencephalon
Mesencephalon
The midbrain or mesencephalon is a portion of the central nervous system associated with vision, hearing, motor control, sleep/wake, arousal , and temperature regulation....
. 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 TS are selective to whether the frequency difference is positive or negative; any given sign-selective cell will fire in one case but not for the other.
Output
Sign-selective cells input into the nucleus electrosensorius (nE) in the diencephalonDiencephalon
The diencephalon is the region of the vertebrate neural tube which gives rise to posterior forebrain structures. In development, the forebrain develops from the prosencephalon, the most anterior vesicle of the neural tube which later forms both the diencephalon and the...
, which then projects onto two different pathways. Neurons selective for a positive difference (stimulus > EOD) stimulate the prepacemaker nucleus (PPn-G), while neurons selective for a negative difference (stimulus < EOD) inhibit the sublemniscal prepacemaker nucleus (sPPn). These prepacemaker nuclei, PPn-G and sPPn, send projections to the pacemaker nucleus (Pn), which ultimately controls the frequency of the EOD.
Pathway in Gymnarchus
The neural pathway of JAR in the African 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 responds over a narrower range of intensities.In Gymnarchus, phase differences between EOD and stimulus are calculated in the electrosensory lateral line lobe (ELL) rather than in the torus semicircularis (TS).
Phylogeny and Evolution
There are two main ordersOrder (biology)
In scientific classification used in biology, the order is# a taxonomic rank used in the classification of organisms. Other well-known ranks are life, domain, kingdom, phylum, class, family, genus, and species, with order fitting in between class and family...
of weakly electric fish, Gymnotiformes
Gymnotiformes
The Gymnotiformes are a group of teleost bony fishes commonly known as the Neotropical or South American knifefishes. They have long bodies and swim using undulations of their elongated anal fin...
from South America
South America
South America is a continent situated in the Western Hemisphere, mostly in the Southern Hemisphere, with a relatively small portion in the Northern Hemisphere. The continent is also considered a subcontinent of the Americas. It is bordered on the west by the Pacific Ocean and on the north and east...
and Osteoglossiformes
Osteoglossiformes
Osteoglossiformes is a relatively primitive order of ray-finned fish that contains two sub-orders, the Osteoglossoidei and the Notopteroidei. All of the living species inhabit freshwater...
from Africa
Africa
Africa is the world's second largest and second most populous continent, after Asia. At about 30.2 million km² including adjacent islands, it covers 6% of the Earth's total surface area and 20.4% of the total land area...
. Electroreception
Electroreception
Electroreception is the biological ability to perceive natural electrical stimuli. It has been observed only in aquatic or amphibious animals, since water is a much better conductor than air. Electroreception is used in electrolocation and for electrocommunication.- Overview :Electroreception is...
most likely arose independently in the two lineages. Weakly electric fish are either pulse-dischargers or wave-dischargers; most are pulse-dischargers, which do not perform the JAR. Wave-discharge evolved in two taxa: 1) the superfamily Apteronotoidea (order Gymnotiformes
Gymnotiformes
The Gymnotiformes are a group of teleost bony fishes commonly known as the Neotropical or South American knifefishes. They have long bodies and swim using undulations of their elongated anal fin...
), and 2) the species Gymnarchus niloticus
Gymnarchus niloticus
Gymnarchus niloticus – commonly known as the aba, aba aba, frankfish, freshwater rat-tail or African knifefish – is an electric fish, and the only species in the genus Gymnarchus and the family Gymnarchidae within the order Osteoglossiformes...
(order Osteoglossiformes
Osteoglossiformes
Osteoglossiformes is a relatively primitive order of ray-finned fish that contains two sub-orders, the Osteoglossoidei and the Notopteroidei. All of the living species inhabit freshwater...
). Notable genera
Genus
In biology, a genus is a low-level taxonomic rank used in the biological classification of living and fossil organisms, which is an example of definition by genus and differentia...
in Apteronotoidea that perform JAR include Eigenmannia
Glass knifefish
Glass knifefishes are fishes in the family Sternopygidae in the order Gymnotiformes. Species are also known as rattail knifefishes.These fishes inhabit freshwater streams and rivers in Panama and South America...
and Apteronotus
Apteronotus
Apteronotus is a genus of weakly electric knifefish in the family Apteronotidae, distinguished by the presence of a tiny caudal fin.-Species:* Black ghost knifefish, Apteronotus albifrons ....
.
Though they evolved the JAR separately, the South American and African taxa have convergently evolved
Convergent evolution
Convergent evolution describes the acquisition of the same biological trait in unrelated lineages.The wing is a classic example of convergent evolution in action. Although their last common ancestor did not have wings, both birds and bats do, and are capable of powered flight. The wings are...
nearly identical neural computational mechanisms and behavioral responses to avoid jamming, with only minor differences.