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15.9I: Electric Organs and Electroreceptors - Biology

15.9I: Electric Organs and Electroreceptors - Biology


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At rest, the interior of each electrocyte, like a nerve or muscle cell, is negatively charged with respect to the two exterior surfaces. The potential is about 0.08 volt, but because the charges alternate, no current flows. When a nerve impulse reaches the posterior surface, the inflow of sodium ions momentarily reverses the charge just as it does in the action potential of nerves and muscles. (In most fishes, electrocytes are, in fact, modified muscle cells.) Although the posterior surface is now negative, the anterior surface remains positive. The charges now reinforce each other and a current flows just as it does through an electric battery with the cells wired in "series".

With its several thousand electrocytes, the South American electric eel (Electrophorus electricus) produces voltages as high as 600 volts. The flow (amperage) of the current is sufficient (0.25–0.5 ampere) to stun, if not kill, a human. The pulse of current can be repeated several hundred times each second.

Powerful electric organs like those of the electric eel are used as weapons to stun prey as well as potential predators.

The Mechanism

In the 5 December 2014 issue of Science, Kenneth Catania describes his experiments that revealed how the electric eel captures its prey.

While exploring its environment, the eel emits a continuous series of low-voltage discharges. Periodically it interrupts these with a discharge of 2 or 3 high-voltage pulses. These cause nearby prey, e.g. a fish, to twitch. Within a tiny fraction of a second (20–40 ms) of detecting the twitch, the eel unleashes a volley (~400 per second) of high-voltage discharges that stun the prey enabling the eel to capture it.

Remarkably, both the twitch response and the immobilization are triggered by the prey's own motor neurons. A pair of pulses induces a brief contraction while a volley of discharges induces tetanus.

Although action potentials in the prey's motor neurons were not measured directly, two pieces of evidence support this mechanism.

  1. The responses remained intact even when the brain and spinal cord of the prey were destroyed thus eliminating the possibility that the prey was relying on a sensory→cns→motor reflex.
  2. Curare, which blocks the transmission of action potentials across the neuromuscular junction did block the prey's responses.

So hunting by the electric eel involves a preliminary 2 or 3 powerful pulses to - in Catania's words - answer the question "Are you living prey?". If the answer is "yes", the prey is quickly stunned and ready to eat.

Weak Electric Organs

The electric organs of many fishes are too weak to be weapons. Instead they are used as signaling devices.

Many fishes, besides the electric eel, emit a continuous train of electric signals in order to detect objects in the water around them. The system operates something like an underwater radar and requires that the fishes also have electroreceptors (which are located in the skin). The presence of objects in the water distorts the electric fields created by the fish, and this alteration is detected by the electroreceptors.

Electric fishes use their system of transmitter and receiver for such functions as

  • navigating in murky water and/or at night
  • locating potential mates
  • defense of their territory against rivals of the same species
  • attracting other members of their species into schools

Electroreception

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Electroreception, the ability to detect weak naturally occurring electrostatic fields in the environment. Electroreception is found in a number of vertebrate species, including the members of two distinct lineages of teleosts (a group of ray-finned fishes) and monotremes (egg-laying mammals). Bumblebees also are able to detect weak electric fields. In vertebrates electroreception is made possible through the existence of sensitive electroreceptor organs in the skin.

Electroreception facilitates the detection of prey or other food sources and objects and is used by some species as a means of social communication. In general, terrestrial animals have little use for electroreception, because the high resistance of air limits the flow of electric current. Thus, humans lack electroreceptors however, through the indiscriminant stimulation of sensory and motor nerve fibres, humans are able to detect strong electric currents (e.g., from batteries or static generators) resulting from either direct contact with an electric source or indirect contact with a conducting medium such as water.


AskNature

Some living systems use electric or magnetic signals as a way to receive information from their environment. Magnetic and electric fields can help such living systems determine direction, altitude, or location, and electric fields also help living systems find other living systems. Detecting and interpreting electrical and magnetic signals requires specialized techniques. For example, mud‑dwelling bacteria use crystals composed of magnetite to sense geomagnetism, which helps orient the bacteria to burrow deeper into the mud.

Class Agnatha (“without jaws”), Class Chondrichthyes (“cartilage fish”), Superclass Osteichthyes (“bone fish”): Sharks, eels, snapper, hagfish

The fish are a diverse group, comprising multiple classes within Phylum Animalia. The most well-known classes are Chondrichthyes, which has sharks and rays, and superclass Osteichthyes, which has all bony fish like cod and tuna. Unlike other vertebrates, fish only live in water. They use special adaptations like fins, gills, and swim bladders to survive. Most are ectothermic, meaning their body temperature depends on the water temperature around them. Over half of all vertebrates are fish. They’re found from the bottom of the sea to high mountain lakes.

The snout of a great white shark detects minute electrical currents produced by prey using electrosensitive organs called ampullae of Lorenzini.

All living organisms generate electric fields around their bodies, but only some organisms are able to sense them. The Elasmobranchii, which includes sharks, rays, and skates, is one group of animals that possesses electroreceptors enabling them to detect electric fields. These fishes use their ability to perceive electric stimuli to hone in on live prey, after their senses of smell and sight have aided them in the initial search.

An elasmobranch electroreceptor, also called an ampulla of Lorenzini (named after the scientist who first described them), consists of a tubular, insulated canal connecting a pore on the surface of the skin to an internal round sac (ampulla). The canal and ampulla are filled with a gel that readily conducts electric currents from the water outside the pore to receptor cells within the wall of the ampulla. These receptor cells are stimulated by the electric current and send signals via nerves to the brain, which integrates the signals arriving from different activated receptors to generate a whole “picture” of the external electric field.

Ampullae of Lorenzini are found around the head in sharks and on the surfaces of the expanded pectoral fins in skates and rays. The pores are visible to the naked eye on the surface of the skin, appearing as small dots.

Learn more about how the ampullae of Lorenzini work in sharks and other elasmobranch fishes in this video by KQED Deep Look.

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Electrolocation and Electrocommunication☆

Central Pathways for Electroreception

Electroreceptors project to a hypertrophied medullary nucleus, the electrosensory lobe (ELL) ( Fig. 3 ). The ELL is a layered structure with separate layers for electroreceptor input, interneurons, principal projection neurons, and feedback/descending input. Electroreceptors terminate in a topographic manner on multiple maps in the ELL of both mormyrid and gymnotiform fish—three maps in mormyrids and four maps in gymnotiform fish. In both types of electric fish, one map is devoted to the ampullary electroreceptors leaving two (mormyrids) and three (gymnotiform fish) maps respectively to process the EA input responsible for electrolocation. In the following I focus on the three maps of the wave type gymnotiform fish, Apteronotus leptorhynchus because the most detailed analyses to date are available for its ELL.

Figure 3 . Simplified schematic of major neuronal pathways of a gymnotiform fish there are similar pathways in mormyrid fish, but there are additional complex pathways related to the corollary discharge to sensory regions that are not illustrated here. Ascending electro-sensory pathways are shown in red, feedback pathways in blue, and electromotor pathways in black. Only the most prominent contralateral projections are indicated. Electroreceptors project topographically onto the ipsilateral electrosensory lateral line lobe (ELL) the presence of three maps is not indicated here. The structure of a major projection neuron, the basilar pyramidal cell, is also indicated the basal dendrite is in receipt of electroreceptor input. The ELL projects to the nucleus praeminentialis (nP) and the midbrain torus semicircularis (TS). The TS in turn projects topographically to the optic tectum (TeO) for control of movements associated with prey capture and navigation. The TS also projects diffusely to the nucleus electrosensorius (nE), a diencephalic region that extracts species-specific electric communication signals. The nE projects to the prepacemaker nucleus (PPn). The PPn also receives extensive additional input from hypothalamic and other brain regions and initiates electric communication signals by modulating the activity of the pacemaker nucleus. The PPn projects to the pacemaker nucleus (PM) cells in the PM cause the baseline (unmodulated) electric organ discharge (EOD). The PM projects to electromotor neurons in the spinal cord these in turn project to the electric organ in the tail of the fish to generate the electric field that stimulates the electroreceptors. The nP receives both ascending (ELL) and feedback (TS) electrosensory input. In turn, it provides feedback projections to the ELL these terminate predominantly on the apical dendrites of ELL pyramidal cells. The direct and indirect feedback pathways are not shown.

The three ELL EA maps have the same overall structure but the size and functional tuning vary in a coordinated manner. A large centromedial map has principle cells with small receptive fields (RFs) optimized for high spatial resolution as might be expected, the principle cells are biophysically tuned for the low frequency AMs associated with electrolocation. The lateral map is small and its principle cells have large RFs optimized for high temporal resolution as might be expected, these cells are tuned for the high frequency AMs associated with electrolocation. The presence of multiple topographic maps with spatial and frequency tuning curves is highly relevant to current theoretical analyses of the effect of tuning curves on population coding. In particular, the three ELL maps begin the process of converting the raw EA input into a sparse code for specific perceptual features such as chirps, envelopes and object motion.

The principal cells of all three maps are mainly pyramidal cells (PCs) with both basal and apical dendrites. The basal dendrites can input to electroreceptors in a small patch of skin is capable of exciting these cells. The apical dendrites receive massive feedback/descending input that modulates in a complex manner the basic coding properties conferred by the EA input. Descending control of sensory processing is a common theme in all sensory systems and the clear separation of feedforward and descending input to basal and apical dendrites of PCs has made them a most useful model system for investigating the role of such modulation.

In the spatial domain, specific types of inhibitory interneurons participate in the generation of surround receptive fields. Thus, many PCs have receptive fields with the center-surround organization very similar to that described for retinal ganglion cells. There is an even more remarkable similarity between retina and ELL. One morphologically defined population of ELL PCs is functionally equivalent to ON center–OFF surround retinal ganglion cells (receptive field center responsive to conductive objects) a morphologically distinct population is functionally equivalent to OFF center–ON surround retinal ganglion cells (receptive field center responsive to nonconductive objects). The ON/OFF cell dichotomy is hard-wired in the biophysics and circuitry of both the ELL and retina and was thought to implement a “labeled line code” for local spatial contrast. It therefore came as shock that, in both ELL and retina, reversing motion of a conductive (bright) object could induce a switch from an ON to OFF cell responding, and vice versa for reversing motion of a nonconductive (dark) object. Both the electro- and visual-sense use a two-dimensional receptor array to extract information about the three dimensional structure of the animal's environment. The ON/OFF switch discovery first indicates that both senses need to implement the ON/OFF switch for the computations required for extracting 3-D reversing motion from 2-D images. These results also raise fascinating but very difficult questions about how downstream circuits can maintain an invariant representation of moving objects despite such a switch in dynamic contrast coding.

Electroreceptor afferents utilize glutamate as a neuro-transmitter, as do most of the feedback/descending pathways to the ELL. Both AMPA-and NMDA-type ionotropic glutamate receptors have been localized in the ELL as well as other regions of the electric fish brain (both gymnotiform and mormyrid). The NMDA receptors of gymnotiform fish have been cloned and found to be highly conserved ELL PCs express high levels of NMDA receptor. As discussed below, this receptor may be critically important in adaptive plasticity of descending and feedback projections to ELL. The dendritic specialization of ELL PCs (basal and apical dendrites receive different inputs) has prompted extensive work on the possible molecular and biophysical correlates of these anatomical differences. In the gymnotiform ELL, there are important differences in the distribution of at least Na + and K + voltage-gated channels on the basal versus apical dendritic trees and perhaps in the distribution of various second messengers as well. Such differential dendritic distribution of ion channels has frequently been reported for pyramidal cells of mammalian cortex, but its functional role remains obscure. In ELL, PC apical dendritic Na + channels mediate a dendritic backpropagating action potential that, in turn, leads to spike bursts. Spike bursts have specific and critical coding properties in the PCs: for example, PC bursts code for object motion in the centromedial map but for fast (chirp) communication signals in the lateral map. Thus, in the gymnotiform ELL, it is possible to directly link dendritic biophysics to sensory computations.

The ELL PCs projects to predominantly contralateral higher brain centers via the lateral lemniscus, a thick myelinated fiber track. There are two main targets: a hindbrain nucleus termed nucleus praeminentialis (nP) and the midbrain torus semicircularis (TS). The nP is involved solely in feedback projections to ELL and is discussed below. The TS is similar to the inferior colliculus of mammals there are far more neurons and neuron types in TS than in ELL. The TS of gymnotiform fish has a complex layered structure, whereas that of mormyrids is organized into discrete nonlayered nuclear groups. For both families of electric fish, the different ELL maps converge in TS.

The TS of gymnotiform fish has been studied in detail. It projects to four target regions: the nP, the optic tectum, the nucleus electrosensorius and the preglomerular nucleus. The projections to the nP imply that higher order electro-sensory processing can influence first-order processing in ELL (since nP is a feedback nucleus projecting back to ELL) this is a common theme in mammalian sensory systems in which cortical sensory areas provide strong feedback to brain stem sensory regions. The exact role of TS to nP feedback projections is not known.

The gymnotiform TS has been intensely investigated with respect to both its morphology and its electrophysiology. There are approximately 50 different cell types in TS and many are now known to be specifically tuned to very different electrosensory signals. Different cell types are specialized for responding to directional object motion versus various communication signals (e.g., beats and chirps). In addition, some cells are tuned to respond selectively to envelope signals (see above) and can presumably implement tracking the motion of conspecifics. The cellular and network bases (e.g., voltage-gated ion channels and synaptic plasticity) of these selective responses are becoming better understood so that, as in ELL, biophysics and network properties can now be directly connected to systems level function. The TS clearly has far more specific tuning than its input ELL pyramidal cells (more sparse coding) synaptic mechanisms by which TS circuits sparsify the ELL input are a key topic of research.

The optic tectum (superior colliculus in mammals) is a highly conserved midbrain nucleus of vertebrates that typically receives retinal input and directs the eyes and body toward salient visual features. It is also typical that other senses, such as touch or audition, project to the deeper layers of the superior colliculus and can therefore also initiate orientation toward these stimuli. It is therefore not surprising that TS (electrosensory) projects topographically to the deeper layers of the gymnotiform tectum and that there are tectal cells which respond to both electrosensory and visual input. Although this has not been studied in depth, it is assumed that the tectum acts as the interface between the electrosensory and motor systems.

The TS projections to the nucleus electrosensorius (a diencephalic brain region) appear to be diffuse (not topographic). Electrophysiological recordings from this nucleus demonstrate that it responds to various types of communication signals, including chirps. Thus, there appears to be a segregation of neural processing by which electrolocation is mediated via the optic tectum, whereas electrocommunication is mediated by the nucleus electrosensorius. The nucleus electrosensorius projects to both the prepacemaker nuclei and hypothalamic nuclei as mentioned above, hypothalamic peptidergic cells then complete the circuit by projecting to the prepacemaker nucleus. The hypothalamic projections to the prepacemaker presumably mediate motivational modulation of electrocommunication but this topic has not been investigated in detail.

The TS and tectum both project to the preglomerular nucleus (PG). The PG of teleost fish is a diencephalic nuclear group that is functionally analogous to the amniote dorsal thalamus: it receives sensory and other input and transmits this input to the dorsal telencephalon (pallium). It is still uncertain whether PG is homologous to thalamus or whether PG/thalamus are examples of convergent evolution. Since both TS and tectum project to PG, electrosensory input associated with navigation and communication can reach the pallium (see below).


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Tuberous receptors

Tuberous receptors are responsible for active electro location– the detection of an electric field produced by the fish’s own electric organs. Therefore, they are only found in those teleost’s that generate an electric organ discharge(EOD), such as the mormyrids, gymnarchids, and mochokidcatfishes of Africa and the gymnotoids of South America. Activeelectro location is limited to freshwater fishes, perhaps because sea water is such a good conductor that maintaining functional sensory field is too difficult.


Schematic diagram of the structure of ampullary (A) and tuberous (B) electro receptive organs. Both organs are surrounded by layers of flattened cells that join tightly to one another. This helps prevent current from bypassing the organs. Tight junctions between the receptor cells and supporting cells help focus incoming electric current through the base of the receptor cells, where they synapse with sensory neurons. Supporting cells in ampullary organs produce a highly conductive gel that fills the canal linking the sensory cells to the surrounding water. Adapted fromHeiligenberg (1993), drawing courtesy of H. A. Vischer.

Tuberous receptors are located in depressions of the epidermis and are covered with loosely packed epithelial cells, allowing electric current to flow between the cells (see Fig. 6.5B). There are at least eight different types of tuberous organs in different species, but they fall into two main categories – those that encode timing of the EOD, and those that encode timulus amplitude (von der Emde 1998).The fish’s EOD frequency causes the tuberous receptor cells and their sensory neurons to generate a rather constant background rate of nerve impulses. A fish can detect objects moving into its electric field (Fig. 6.6) when those objects cause a change in the field and alter the rate of impulses received by the brain, such as when the fish encounters an object with different conductance than the surrounding water. This probably allows the fish to detect the size and distance of the object, and may also permit discrimination between living and nonliving objects because their different electrical properties would create different distortions of the electric field.


Active electroreception is used in a variety of ways. Many electric fishes are primarily nocturnal and use theirelectro sensory capabilities to locate hiding places during the day and to explore their environment at night (von derEnde 1998 Graff et al. 2004). Active electroreception also can be used to locate prey and assist with navigation and orientation, especially because the fish are most active during periods of low or no light. But the most studied use of active electroreception is in communication.


A BIOLOGICAL FUNCTION FOR ELECTRORECEPTION IN SHARKS AND RAYS

Carl D. Hopkins discusses Adrianus J. Kalmijn's 1971 paper entitled ‘The electric sense of sharks and rays’.

Carl D. Hopkins discusses Adrianus J. Kalmijn's 1971 paper entitled ‘The electric sense of sharks and rays’.

The discovery of a new sensory modality in animals is of great significance in the history of biology – akin to the description of a new species of bird or primate or the unearthing of a missing link in the fossil record. In this issue we celebrate one of the key papers in the discovery of electroreception in fishes (Kalmijn, 1971), which established a biological function for the ampullae of Lorenzini in sharks and rays. It has become a citation classic for The Journal of Experimental Biology.

Evidence for electroreception accumulated rapidly in the period between 1957 and 1971. First, there were behavioral studies that showed that weakly electric fish from Africa and South America could communicate with conspecifics (Möhres, 1957) and ‘electrolocate’ hidden objects in their environment (Lissmann and Machin, 1958). Electrolocation in electric fish had much in common with echolocation in bats that were using ultrasound to find their insect prey (Griffin, 1958). These fishes could sense objects that differed in conductivity from the water even when visual, chemical and mechanical cues were obscured. Shortly after Lissmann and Machin's behavior study in 1958 (Lissman and Machin, 1958), which is also a JEB Classic (Alexander, 2006), came electrophysiological recordings from electroreceptors (Bennett, 1965 Bennett, 1971 Bullock et al., 1961 Fessard and Szabo, 1961 Murray, 1959 Murray, 1960 Murray, 1962), anatomical studies on the receptor organs (Bennett, 1965 Bennett, 1971 Derbin and Szabo, 1968 Szabo, 1965) and neurobiological studies of sensory coding (Bullock and Chichibu, 1965 Hagiwara and Morita, 1963 Hagiwara et al., 1962 Hagiwara et al., 1965a Hagiwara et al., 1965b).

Despite this rapid progress it was still unclear how the earliest electroreceptors evolved because there had been no study of the functional role of electroreception in species lacking weak electric organs. This included the non-electric sharks, skates and rays, and catfish and, as we now know, many others (Bullock and Heiligenberg, 1986 Bullock and Hopkins, 2005 Bullock et al., 2005 Hopkins, 2009). These electroreceptive but non-electric fishes were obviously the key to solving Darwin's (Darwin, 1859 Darwin, 1872) ‘case of special difficulty’ – the origin of electric organs in electric eels and Torpedo rays through a series of gradual adaptive modifications. If weak electric organs were useful for both communication and active electrolocation, it was possible to conceive of the intermediate steps that would lead to the evolution of stronger and stronger electric organs. But what was the function of electroreceptors if electric organs were absent, as they are in sharks and most rays?

In 1971 in one short paper, now a JEB Classic article, Adrianus J. Kalmijn from the University of Utrecht in The Netherlands found the answer. He demonstrated that these elasmobranchs could detect natural electric fields surrounding fish that were their natural prey, that they could orient to these electric fields, and that they could accurately attack them even when their prey was visually hidden – as occurred when the flatfish Pleuronectes platessa was buried under the sand. They could do so, at night, and even when chemical and mechanical cues were absent. The experiments were simple and clear, and the writing was direct. Furthermore, this paper had one memorable figure – a ‘story board’ for the six experiments performed in the study – that sticks in your mind like a Mozart melody. It lays out the evidence for a natural function for these electroreceptors (see Fig. 1 legend). By establishing a clear natural function for electroreception, Kalmijn did what Parker and van Heusen (Parker and van Heusen, 1917) had not done in their earlier account of experiments showing that catfish respond to metallic rods and galvanic currents. Prey capture was not simply a curious perceptual response of an animal in an experimental set-up but a natural sensory response essential to its survival. Hence, it was a new sense organ.

Kalmijn's behavioral experiments revealed the importance of electroreception in passive electrolocation of prey (Kalmijn, 1971). The studies were conducted in captivity, and the spotted dogfish shark Scyliorhinus canicula detects and accurately attacks its natural prey, a flatfish, Pleuronectes platessa, buried under the sand (A). The shark also attacks when the flatfish is covered both by sand and a chamber molded from agar made with seawater (B). The sand blocks visibility of the prey while the agar chamber impedes mechanical cues due to water motion and limits diffusion of chemicals but it has the same electrical conductivity as the seawater. By pumping water through the chamber to an exit tube some distance away, Kalmijn tested the importance of chemical cues carried in from the water flow (Kalmijn, 1971). The shark attacks the chamber, not the outflow. Chopped fish bait under the agar chamber redirects the shark's attack to the outflow tube (C). Electrically insulating the agar chamber with thin plastic sheeting blocks the flatfish's inevitable bioelectric signals and muscle potentials and the shark is disoriented (D). As proof that the shark is guided by the electric signal, electrodes buried in the sand replace the prey, and when they are connected to a low frequency 4 μA current source emitting signals that are close in amplitude to natural bioelectric emissions (ca. 120 μV 5cm −1 , 1 Hz sine wave) the shark attacks (E). Finally, the sharks show a preference for attacking the electrodes even if a piece of fish bait is presented on the surface (F). Reprinted from fig. 2 from Kalmijn (Kalmijn, 1971).

Kalmijn's behavioral experiments revealed the importance of electroreception in passive electrolocation of prey (Kalmijn, 1971). The studies were conducted in captivity, and the spotted dogfish shark Scyliorhinus canicula detects and accurately attacks its natural prey, a flatfish, Pleuronectes platessa, buried under the sand (A). The shark also attacks when the flatfish is covered both by sand and a chamber molded from agar made with seawater (B). The sand blocks visibility of the prey while the agar chamber impedes mechanical cues due to water motion and limits diffusion of chemicals but it has the same electrical conductivity as the seawater. By pumping water through the chamber to an exit tube some distance away, Kalmijn tested the importance of chemical cues carried in from the water flow (Kalmijn, 1971). The shark attacks the chamber, not the outflow. Chopped fish bait under the agar chamber redirects the shark's attack to the outflow tube (C). Electrically insulating the agar chamber with thin plastic sheeting blocks the flatfish's inevitable bioelectric signals and muscle potentials and the shark is disoriented (D). As proof that the shark is guided by the electric signal, electrodes buried in the sand replace the prey, and when they are connected to a low frequency 4 μA current source emitting signals that are close in amplitude to natural bioelectric emissions (ca. 120 μV 5cm −1 , 1 Hz sine wave) the shark attacks (E). Finally, the sharks show a preference for attacking the electrodes even if a piece of fish bait is presented on the surface (F). Reprinted from fig. 2 from Kalmijn (Kalmijn, 1971).

Why was this paper so compelling, given that most of the basic anatomy of electroreceptors was known by 1971, and most of the functions already established? Perhaps it was the care with which the laboratory studies were linked to relevant field conditions, or the clarity of the figure, or the economy of the writing, which summarized data without tables or statistics. I first met Ad Kalmijn in Ted Bullock's laboratory at Scripps Institution of Oceanography in San Diego, CA, USA, shortly after this paper was published. It was a good time to be a post-doc there, as the Bullock lab was thriving with several students and post-docs actively at work on electroreception and other aspects of comparative neurobiology. Walter Heiligenberg had just arrived to study the Jamming Avoidance Response, and Joe Bastian was trying to understand the large cerebellum of electric fish. Kalmijn was busy setting up large tanks for testing sharks and rays. He helped Eric Knudsen, a beginning graduate student, to study electroreception and the geometry of electric fields from weakly electric fish. Knudsen later made electrophysiological recordings of sensory maps for electric field vectors in the torus semicircularis of catfish. Several years later Kalmijn wrote influential papers on the use of electroreceptors in the detection of the Earth's magnetic field (Kalmijn, 1974), which he alluded to in his JEB paper and he was influential in understanding the physics of electric and hydrodynamic fields in water (Kalmijn, 1997). It was an exciting time to work on the many aspects of this new sensory modality, and it is gratifying to see how far electric fish have come, from those early beginnings to become a great model system in neuroethology (Bullock et al., 2005).

I often return to Kalmijn's 1971 paper in my teaching. I show Fig. 1 and tell the story of how we learned the function of early electroreception in fishes.


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Electroreceptors of a weakly electric fish

The hypothesis of an active electroreceptor filter, characterized by an underdamped, oscillatory impulse response, was tested indirectly by investigating the pattern of afferent discharges resulting from receptor excitation with electric field pulses. When stimulated with a single, high amplitude, short duration pulse the majority of afferents responded with bursts of two or three spikes having interspike intervals, in individual fish, correlated to the individual's electric organ discharge period, and, more importantly, with the best frequency of the corresponding receptor. Pulses causing current to flow into the receptor from the bath resulted in shorter response latencies and more spikes per burst than pulses of the opposite polarity. The polarity dependent latency shift was also correlated with the best frequency of the receptor and the electric organ discharge repetition rate of an individual, but it was much shorter than expected based on the prediction of a generator potential in the form of a classical underdamped oscillation. Because of this it is concluded that the generator potential oscillations increase in period for successive cycles. This was essentially confirmed by the form of the receptor organ excitability cycle which was measured by using a two pulse stimulus paradigm.

Further confirmation of the existence of an oscillatory generator potential was obtained by recording compound action potentials from the afferent nerve and comparing the single peaked potentials obtained by direct nerve shock with the multipeaked potentials evoked by receptor activity in response to electric field pulses in the water.

The physiological properties of tuberous electroreceptors are nearly the same as the properties of receptors in the phylogenetically related vertebrate auditory system. This leads to the suggestion that the two systems have in common similar physiological mechanisms, and that the oscillatory receptor properties observed for electroreceptors may serve, in the auditory system, as the basis for a proposed second filter.


Electroreceptors in the platypus

It has been known since the last century that the bill of the platypus contains densely packed arrays of specialized receptor organs and their afferent nerves. Until recently these were thought to be largely mechanoreceptive in function. However Scheich et al. 1 provide both behavioural and electrophysiological evidence that there are electroreceptors in the bill of the platypus. These authors were able to record evoked potentials from the somatosensory cortex of the brain in response to weak voltage pulses applied across the bill. Behavioural observations showed that a platypus could detect weak electric dipoles and it was suggested the animal was able to locate moving prey by the electrical activity associated with muscle contractions. From these observations, and in view of the fact that it was known that the bill contained gland receptors 2 which in several respects resembled the ampullary electroreceptors in freshwater fish, Scheich et al. concluded that the receptor array of the platypus bill included electroreceptors. In this report we present direct electrophysiological evidence for the existence of such receptors.


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In: Fish Physiology , Vol. 5, No. C, 01.01.1971, p. 493-574.

Research output : Contribution to journal › Article › peer-review

N1 - Funding Information: I am indebted to Dr. R. B. Szamier for many of the morphological figures. Supported in part by grants from the National Institutes of Health (5 PO1 NB 07512 and HD-04248) and the National Science Foundation (GB-6880).

N2 - Many groups of fish have receptors that are specialized for the detection of electric fields. The existence of these electroreceptors was first clearly indicated in weakly electric fish, which continually set up low voltage electric fields around themselves by means of their electric organs. If the water over a receptor opening is replaced by air, a local electrode need pass much less current to produce a given voltage change outside the receptor the shunting by the water is reduced. Although the degree of residual shunting by the skin and remaining water has not been satisfactorily evaluated, the current voltage relation measured under these conditions is likely to have considerable contribution from the receptor cells because the input resistances become large, as high as several megohms. Receptor cells of phasic receptors contribute importantly to the external potentials under these conditions. Another important characteristic of the input–output relationship of the receptor synapses is sensitivity. The input–output relationship of synaptic membrane of phasic receptor cells differs from that of tonic receptor cells in that there is little resting release of transmitter. It is difficult to be confident of the shape of the potential-secretion relationship because of active processes in the receptor cells. It is likely but uncertain that the secretory membrane of phasic receptors does have an input–output relationship that has a much greater slope than that at known interneuronal and neuromuscular synapses.

AB - Many groups of fish have receptors that are specialized for the detection of electric fields. The existence of these electroreceptors was first clearly indicated in weakly electric fish, which continually set up low voltage electric fields around themselves by means of their electric organs. If the water over a receptor opening is replaced by air, a local electrode need pass much less current to produce a given voltage change outside the receptor the shunting by the water is reduced. Although the degree of residual shunting by the skin and remaining water has not been satisfactorily evaluated, the current voltage relation measured under these conditions is likely to have considerable contribution from the receptor cells because the input resistances become large, as high as several megohms. Receptor cells of phasic receptors contribute importantly to the external potentials under these conditions. Another important characteristic of the input–output relationship of the receptor synapses is sensitivity. The input–output relationship of synaptic membrane of phasic receptor cells differs from that of tonic receptor cells in that there is little resting release of transmitter. It is difficult to be confident of the shape of the potential-secretion relationship because of active processes in the receptor cells. It is likely but uncertain that the secretory membrane of phasic receptors does have an input–output relationship that has a much greater slope than that at known interneuronal and neuromuscular synapses.


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