An Electric Sense for an African Electric Fish By Carl D. Hopkins Tuberous electroreceptors are sensitive to Section of Neurobiology and Behavior AC stimuli with frequencies above 100 Hz, Cornell University, Ithaca, NY but not to D.C. stimulation. They lack the The electric fish in this demonstration belong to the family Mormyridae, canal to the surface. Instead, there is a loose the “elephant-snouted” or “weakly-electric” fish endemic to Africa. All plug of epithelial cells leading to the skin of the mormyrids have a well-developed electric sense that is used for surface. The receptor cells lie buried under communication and for active and passive electrolocation. The skin of the skin surface. The nerve impulses are usu- From Szabo, 1965 these fish is covered with electroreceptors of three different types. The ally silent, but respond to electrical transients, demonstration illustrates recordings of electrical action potentials from such as the on or off of an electrical stimulus. one of these, the Knollenorgan electroreceptor, which functions as a frequency-tuned communication sensor and as a time-coder. In mormyrids, there are two types of tuberous organs: Electroreception: a sensory modality known to exist only for cer- Knollenorgans are highly sensitive to the electric discharges from tain aquatic vertebrates. It provides an ability to detect weak elec- the electric organs of other mormyrids. First, they are tuned to the tric currents in water. The origin of sensitivity may be traced to frequencies where there is the most energy in the EOD. Second, sense organs located in the skin of the animals. they are the most sensitive of the tuberous organs. Curiously, when Electroreception is limited to aquatic environments probably be- a mormyrid fish discharges its electric organ, it never ‘hears’ itself cause only in water is the resistance of the environment low enough on its Knollenorgan, because a neural circuit in the brain blocks the to allow electric currents to flow. By detecting electric currents, sensory response just at the precise mo- electroreceptive organisms enjoy the benefits of a sixth sense -- a ment when the fish is expecting to receive new window on the world -- that is unavailable to terrestrial ani- its own discharge. Because the mormyrid mals that live in the medium of air. fish can detect other fish but not itself with these sense organs, we say that the Electroreceptors are widespread in primitive (non-teleost) fishes, as Knollenorgan is a “communication sen- well a few isolated cases of teleosts such as the ones demonstrated sor”. here. They are also known for aquatic salamanders and caecilians, From Szabo, 1965 and in at least one species of mammal, the Duck-Billed Platypus. It Knollenorgans are composed of a set of is generally believed to be an ancient sensory modality that is re- receptor cells (RC) which may reach 40 to 60 microns in diameter. lated to, and perhaps derived from, the lateral line sense. Of all the A single, heavily myelinated nerve with a large diameter inner- senses, electroreception is closest in function to that of hearing. vates several receptor cells. The synapse between receptor cell and Mammalian electroreceptors evolved independently from the sense nerve terminal is electrical, not chemical. One to eight receptor organs of fishes. cells are found in each organ. There is a loose plug of epithelial cells between the tuberous organ and the skin surface. The outer Thresholds for sensing electric fields in water can be as low as 0.01 surface of the Knollenorgan sensory cell is covered with dense microvolts per cm for some species of fish. The most sensitive are layer of microvilli, increasing its surface area enormously. the sharks and rays that have Ampullae of Lorenzini. Most elec- troreceptors are rather insensitive to mechanical, light, chemical, Mormyromast receptors in mormyrids are also sensitive to AC and temperature changes. There are specific behaviors associated stimuli, but they have a much higher threshold compared to Knol- with electroreception, which include prey detection and predator lenorgans. They too are silent if unstimulated, and respond only avoidance. For those fishes with specialized electric organs, elec- when an electrical stimulus, like the EOD, is present, and quite troreception is also used for active object location and social com- strong. The mormyromast functions in sensing objects in the munication. It has been proposed that electroreceptors in sharks fish’s environment in a process known as active electro-location. and rays could be used to detect the earth’s magnetic field (by the As objects that differ in conductivity from the water distort the electric fields that are induced when the shark swims through the electric field generated by the EOD, the fish detects the distortions magnetic field lines). and learns about the location, size, distance, and resistance and capacitance of the object. Types of Electroreceptors Physiological Characteristics. Knollenorgans respond to outside- For those very special and unusual “electric” fishes that can gener- positive-going transients in electrical stimulation. They fire on the ate weak electric discharges, there are known to be three different positive going edge of a square wave stimulus, whether the edge is types of electroreceptors. This applies to both the South America the “on” edge of a positive square wave or the “off” of a negative Gymnotiformes and Africa Mormyridae, square wave. which are biologically distantly related and Most Knolle- share no common electrogenic ancestor. norgans have Ampullary electroreceptors are most sensitive some irregular to D.C. electric fields. The receptors have an spontaneous ac- From Bennett, 1971. S = stimulus waveform, RP = receptor tivity that may be potential from a Knollenorgan; NP = action potential in the “ampoule-shaped” canal that leads to the skin afferent nerve. surface; the sensory cells lie at the base of the suppressed by canal. Ampullary receptors are spontane- outside-negative-going transients. Firing probability goes from ously active but modulate the rate of nerve From Szabo, 1965 R.C. = silence to 1 to 1 firing over a dynamic range of 10 decibels. The receptor cell; b.m. = basement Knollenorgan spike causes the afferent nerve to fire a spike with impulses up or down in response to posi- membrane; n = nerve. tive or negative electric stimuli. a short (0.2 ms) delay. Receptor and afferent are coupled by an gram of spike latencies for a single Knollenorgan firing spikes in electrotonic synapse. response to an EOD. The compound action potentials cement to- gether the responses to the Central projections of the afferent nerve. The Knollenorgan af- normal and inverted EOD to ferents travel in the lateral line nerve to the posterior lateral line make a single histogram lobe of the hindbrain, also known as the electrosensory lateral line with both polarities. lobe (ELL). The ELL is unique to electro- Tuning Curves. Like receptive fishes, but it auditory receptors and ves- is similar in structure tibular receptors, the Knol- to the cochlear nuclei lenorgan receptors are tuned From Amagai et al, in press. that receive afferent to electrical stimuli. Typi- nerves from the audi- cally these receptors are tory periphery, and to most sensitive to frequencies in the 500 Hz to 2000 Hz range, but the hindbrain nuclei the best frequency varies between species depending upon the which receive lateral spectrum of energy in the species-typical EOD waveform. Those line and other mecha- fish with short duration EODs have most of the electrical energy at nosensory fiber inputs. high frequencies and the Knollenorgans are correspondingly tuned Electroreceptor affer- to high frequencies while those with longer EODs have Knollenor- ents terminate on somata of large spherical cells in the nucleus of gans tuned low. We can assess the tuning range for Knollenorgans the lateral line lobe (nELL) with large calyx-like synaptic termi- by presenting sine waves to the receptor and estimating the thresh- nals. The large spherical cells project to the nucleus exterolateralis old amplitude at a range of different frequencies. pars anterior (ELA) of the midbrain via the lateral lemniscus. The References spherical cells in the nELL receive inhibitory inputs from the command-associated nucleus. This input blocks the spike in the Amagai, S., Friedman, M. A. and Hopkins, C. D. (in press). Time-coding in the spherical cell at precisely the moment when the fish expects to re- midbrain mormyrid electirc fish I: Physiology and anatomy of cells in the nucleus exterolateralis pars anterior (ELa). Journal of Comparative Physiology A . ceive the sensory response from its own EOD. As a consequence, the fish is electrically ‘deaf’ to its own discharge but it can detect Bennett, M. V. L. (1965). Electroreceptors in mormyrids. Cold Spring Harb. Symp. the EODs of other fish in its vicinity. Quant. Biol. 30, 245-262. Bennett, M. V. L. (1971). Electroreception. In Fish Physiology, vol. V (ed. W. S. Recording Action Potentials from Knollenorgan Receptors In Hoar and D. J. Randall), pp. 347-491. New York: Academic Press. this demonstration we record the spike-like action potentials from Bullock, T. H. and Heiligenberg, W. (1986). Electroreception. In Wiley Series in the receptor cells of the Knollenorgan receptor of mormyrids by Neurobiology (ed. R. G. Northcutt). New York: John Wiley & Sons Inc. placing a fine wire next to the receptor opening. The wire is at- tached to a bridge-amplifier capable of recording the 1 to 10 mV Fessard, A. and Szabo, T. (1961). Mise évidence d'un récepteur sensible à l'élec- tricité dans la peau d'un mormyre. C. rendu hebd. Séanc. Acad. Sci. Paris 253, 1859- action potentials from the receptor pore while simultaneously de- 1860. livering a stimulus to the pore. Stimulation and recording is ac- Hopkins, C. D. (1983). Sensory mechanisms in animal communication. In Animal complished through a bridge circuit, which allows us to pass cur- Behaviour 2: Animal Communication, vol. 2 (ed. T. R. Halliday and P. J. B. Slater), rent through the same electrode used for recording action poten- pp. 114-155. Oxford: Blackwell Scientific Publications. tials. Balancing the bridge circuit and canceling the artifact nulls Hopkins, C. D. (1986). Behavior of Mormyridae. In Electroreception (ed. T. H. the stimulus artifact out. This method was first used by Michael Bullock and W. F. Heiligenberg), pp. 527-576. New York: John Wiley & Sons. V.L. Bennett and by Szabo, who first recorded electrical activity from Knollenorgans. Hopkins, C. D. (1988). Neuroethology of electric communication. Ann. Rev. Neuro- sci. 11, 497-535. Knollenorgan receptor spikes fire on the positive-going transient Hopkins, C. D. (1995). Convergent designs for electrogenesis and electroreception. edges of electrical stimuli. There is a delay of 0.2 ms before the Current Opinion in Neurobiology 5, 769-777. spike in afferent nerve. In response to a sine-wave stimulus, Hopkins, C. D. and Westby, G. W. M. (1986). Time domain processing of electric Knollenorgans fire at or near the zero crossing of the waveform and organ discharge waveforms by pulse-type electric fish. Brain Behavior and Evolu- phase lock to the stimulus. tion 29, 77-104. Temporal Coding of EODs. The electric organ discharges Lissmann, H. W. and Machin, K. E. (1958). The mechanisms of object location in Gymnarchus niloticus and similar fish. Journal of Experimental Biology 35, 457- (EODs) of mormyrids are complex pulse-like waveforms that act as 486. species-typical and sex-specific signatures. Each species has its own characteristic EOD waveform that may be a unique signature Szabo, T. (1965). Sense organs of the lateral line system in some electric fish of the Gymnotidae, Gymnarchidae, and Mormyridae. J. Morphology. 117, 229-250. within a given ecological niche. There may be some species that do not have unique EODs. Knollenorgans respond to the EOD This demonstration was prepared for the Howard Hughes Medical waveform by firing one or two spikes at specific latencies within Institute “Senses and Sensitivity” lectures, December 8-9, 1997 by the stimulus waveform. Although a single Knollenorgan fires only the generous contributions of Mr. Peter Lovell, NIH fellow in on one polarity of the stimulus, those organs on different parts of Neurobiology and Behavior at Cornell University; by Mr. Garry the body may respond to the inverse polarity as the current flows Harned, Research Support Specialist at NBB at Cornell; and Dr. through the receiver fish’s body, in one side and out the other. Satoshi Amagai, HHMI. Thus, a population of Knollenorgans may encode both polarities of the stimulus. The diagram below illustrates a compound histo-