Sixth Sense Abcderium

by Brian L. Keeley

Electroreception is the ability to perceive the world via electricity. This non-human sense has been discovered in many fishes and other animals.¹ Where sighted organisms can perceive variations in photonic energy due to their possessing eyes and hearing organisms can perceive variations in vibratory energy due to their possessing mechanoreceptive organs, such as the mammalian cochlea, electroreceptive organisms possess dedicated sensory organs that allow them detect variations in the electrical properties of their environments.  Although German physiologist and zoologist, Johannes Müller (1801-1858), had hypothesized the existence of an electrical sense as early as the 1830s, it would take until the 1960s before sufficient evidence had been amassed to generate a scientific consensus that the electrical modality had been demonstrated.

Historical background²

As long ago as ancient Egypt, humans have been familiar with the phenomenon of animal electricity. The electric catfish of the Nile (Malapterurus electricus) is featured in Egyptian murals and statuary. Hippocrates, Plato, and Aristotle were all familiar with the stunning charge of Torpedo ocellata, a Mediterranean species of ray from which the modern English words “torpor” and “torpid” derive their meanings. Even prior to the development of the modem theory of electricity in the eighteenth century, it was recognized that there was something unusual about certain kinds of catfish, rays, and eels. In addition, in the nineteenth century, “pseudoelectric fish” were discovered in the waterways of Africa and South & Latin America that possessed tiny organs similar to those of the larger, electric eels, but which produced no discharge strong enough to be detected by the naked hand. Soon after the discovery of ways to detect and measure electricity in the late nineteenth century, the true nature of these bioelectric animals was revealed (and the “pseudoelectric fish” were thereafter known as “weakly electric fish”).

Eventually, some began to suspect that, in addition to the ability to generate electricity, some animals could detect the presence of electricity in their environment. The electrosensory hypothesis gained credibility in 1911 when George H. Parker and Anne P. van Heusen (1917) discovered that the non-bioelectrogenic catfish, Ictalurus (Amiurus) nebulosus, could detect galvanic and direct currents. They did so through a series of experiments in which they presented blindfolded catfish with glass, wooden, and metal rods. The fish were able to detect the presence of metallic rods at a distance, but only reacted to the glass and wooden rods when the rods touched the surface of the fish. After calculating the likely amount of current produced by the galvanic reaction in the metal rods, they then successfully repeated the experiments using electrodes placed in the water of their aquaria.

Notably, although they had demonstrated a behavioral response to electrical stimulation in their catfish, Parker and van Heusen did not claim to have discovered electroreception. The behavioral response is a necessary condition for positing a sensory modality; it is not sufficient. Instead, they admitted that they could not rule out that their catfish were merely detecting the presence of electricity due to the overstimulation of their taste buds or some other sensory system (much the same way that humans can detect electricity presented directly to the tongue, for example, as when a 9-volt battery is touched to the tip of the tongue). Positing a genuine electrosensory modality required the discovery of some organ dedicated and specifically tuned to the perception of electricity.

In the 1950s, British zoologist Hans Lissmann (1951; 1958; 1958)—himself building on proposals made a decade earlier by C. W. Coates of the New York Aquarium—proposed a mechanism by which an electric fish might detect objects in its environment. He proposed that, “it can be imagined that such a fish, living in a private, electric world of its own, receives a variety of information through sense organs distributed over the surface of its body which may be likened to an ‘electro-receptive retina’” (1958, 186). The existence of such “electro-receptive” sensory organs were finally demonstrated in the 1960s. Theodore “Ted” Bullock and colleagues (1961), recording from the nervous system of different weakly electric fish species, measured differential neurophysiological activity when the fish were stimulated by passing a conductive or insulating object nearby. Significant neural activity was not observed when the fish were stimulated by ecologically-valid levels of mechanical stimulation (brushing the skin with a brush or with weak water currents). They conclude that they had demonstrated the existence of “true electroreceptors.” In the same decade, it was demonstrated that one function of structures, known as the ampullae of Lorenzini, found in sharks, skates and rays (including the Mediterranean Torpedo) was the detection of electrical fields.⁴

The electrical sense

The number of species for which electroreception has been claimed has grown to include salamanders, catfish (including Parker and van Heusen’s catfish), sturgeons, paddlefish, lungfish, lampreys. There is even good evidence for a mammalian electroreceptive species: the platypus (Pettigrew 2004; Scheich et al. 1986).

Electroreception is used in a number of ways by the animals that have this sense.  In the passive electroreceptors—those organisms, such as sharks, catfish and platypus, that can perceive electricity in their environments without producing it themselves—it is used to detect living prey even where it cannot be seen. For example, a well camouflaged flounder under a layer of mud on the bottom of a bay will still give off a detectable electrical signal. Because the electrical signals we are talking about are often very tiny and at some distance from the predator, passive electroreceptors must be very sensitive, with detection thresholds on the order of nanovolts/cm³. Amazonian catfish have been captured and found to have stomachs full of weakly electric fish tails, suggesting that they use their electroreceptive sense to hunt and prey upon active electroreceptors.

As originally proposed by Lissmann, active electroreceptors—various species of weakly and strongly electric fish, such as the electric eel—can detect objects in their environment by perceiving how the electric field they produce around themselves is modified by those objects. To the extent that the conductive properties of objects in the water differ from that of the surrounding water itself, the object will characteristically modulate the electric field as detected at the surface of the fish’s skin (in which the electroreceptive sensory cells are embedded), which Lissmann aptly described as an “electroreceptive retina”.

Finally, many of the weakly electric fish species use their active electroreceptive sense as part of their social behavior.  First, each species of fish has its own characteristic electric organ discharge. Furthermore, in several species the electrical discharge is sexually dimorphic. Therefore, weakly electric fish can use their electrical sense to detect who are their conspecifics.  In addition, many electric fish modulate their electrical discharge during courtship. So, just as in many species of bird, the male will produce a species-specific courtship song in the presence of a sexually-receptive female as part of courtship behavior, the male weakly electric fish will modulate its electric organ discharge as a kind of “electric courtship song” (albeit one of much less apparent complexity from the songs of birds, see (Hagedorn and Heiligenberg 1985)).

Do humans possess this sense? It is unlikely, and to date, there is not much credible evidence that we do. For one thing, all known electroreceptive species are aquatic. Electricity is conducted by water, but is only poorly conducted, if at all, by air. While humans, like all organisms, can be acted upon by electricity—we can suffer electrocution, electroshock, etc.—this does not in itself constitute evidence for the possession of a sense, in the same way as electric fish have it. By way of comparison, consider that most animals, including humans, possess the ability to detect the presence of strong acids, due to the damage such substances can do to our bodies when exposed, but it seems absurd to posit an “acid sense” in us because of that fact.

Humans do possess the ability to detect the presence of electricity in our environment, as with the 9-volt battery scenario described above. This is due to the electrical nature of nerve cells; all organisms with nervous systems can do this.  In the decades after the discovery of “galvanism” (as the phenomenon was originally known), it was a somewhat popular parlor trick or scientific demonstration to discharge electricity around the body. When the discharge is near an eye, a bright light is seen. When the discharge is near an ear, a roar is heard. Near the feet, a tickle is felt. These sensory effects are due to the stimulation of sensory nerve cells by the galvanic discharge. This phenomenon seems importantly different from the sensory abilities of the electroreceptive animals described above, especially those active electroreceptors that generate electricity as a means of sensorily exploring their environments.

Brian L. Keeley

Philosophy, and Science, Technology & Society Field Groups

Pitzer College, Claremont, California

Notes

1.    For a clear discussion of this and other unusual animals senses, see (Hughes 1999,, Part III).

2.    I go over some of this same historical background in (Keeley 1999). Other excellent accounts of the history of the discovery of the electrical sense can be found in (Moller 1995; Moller and Fritzsch 1993).

3.    See also (Keeley 2008).

4.    A more current discussion of the state-of-the-art understanding of electroreception can be found in (Bullock et al. 2005). For an account of the details of how a weakly electric fish brain processes electrical sense input, see (Heiligenberg 1991).

References

Bullock, Theodore H., et al. “Evidence for a Category of Electroreceptors in the Lateral Line of Gymnotid Fishes.” Science 134  (1961): 1426-27. Print.

—, eds. Electroreception. Vol. 21. New York: Springer, 2005. Print.

Hagedorn, M., and Walter Heiligenberg. “Court and Spark: Electric Signals in the Courtship and Mating of Gymnotoid Fish.” Animal Behavior 33  (1985): 254-65. Print.

Heiligenberg, Walter. Neural Nets and Electric Fish. Cambridge, MA: The MIT Press (A Bradford Book), 1991. Print.

Hughes, Howard C. Sensory Exotica: A World Beyond Human Experience. Cambridge, MA: The MIT Press, 1999. Print.

Keeley, Brian L. “Fixing Content and Function in Neurobiological Systems: The Neuroethology of Electroreception.” Biology & Philosophy 14  (1999): 395-430. Print.

—. “Theodore Holmes Bullock (1915-2005).” New Dictionary of Scientific Biography. Ed. Koertge, Noretta. Vol. Volume 1. New York: Charles Scribner’s Sons, 2008. 436-39. Print.

Lissmann, H. W. “Continuous Electrical Signals for the Tail of a Fish, Gymnarchus Niloticus Cuv.” Nature 167  (1951): 201–02. Print.

—. “On the Function and Evolution of Electric Organs in Fish.” Journal of Experimental Biology 35  (1958): 156–91. Print.

Lissmann, H. W., and K. E. Machin. “The Mechanism of Object Location in Gymnarchus Niloticus and Similar Fish.” Journal of Experimental Biology 35  (1958): 451–86. Print.

Moller, Peter. Electric Fishes: History and Behavior. London: Chapman & Hall, 1995. Print.

Moller, Peter, and B. Fritzsch. “From Electrodetection to Electroreception: The Problem of Understanding a Non-Human Sense.” Journal of Comparative Physiology A 173  (1993): 734–37. Print.

Parker, G. W., and A. P. van Heusen. “The Responses of the Catfish, Amiurus Nebulosus, to Metallic and Non-Metallic Rods.” American Journal of Physiology 44  (1917): 405–20. Print.

Pettigrew, John D. “Bi-Sensory, Striped Representations: Comparative Insights from Owl and Platypus.” Journal of Physiology-Paris 98 1-3 (2004): 113. Print.

Scheich, H. G., et al. “Electroreception and Electrolocation in the Platypus.” Nature 319  (1986): 401–02. Print.