Box Extension 20.1

Electric Fish Exploit Modified Skeletal Muscles to Generate Electric Shocks

In addition to using skeletal muscles for locomotion, electric fish have incorporated highly modified skeletal muscle cells—called electrocytes—into electric organs (EOs), which they use for stunning prey, exploring the environment, and communicating. Researchers recently investigated the specific effects on prey of electric discharges produced by the electric eel Electrophorus electricus from freshwater rivers of South America (Figure A). They first showed that high-voltage electric discharges produced by the eel’s EO specifically stimulated the prey’s efferent motor neurons, causing them to release acetylcholine (ACh) at skeletal muscle end-plates. The researchers then demonstrated how the electric eels time the discharges so that they either immobilize free-swimming fish or reveal the locations of hidden fish. When an eel targets free-swimming prey, it emits high-frequency discharges (~400 Hz) that remotely stimulate the prey’s motor neurons at such a high frequency that they cause the skeletal muscles to undergo tetanus and temporarily immobilize the prey. During this short period of immobility, the electric eel captures the prey. To flush out hidden prey, the electric eel emits two or three high-voltage discharges that stimulate the prey’s motor neurons to produce full-body twitches that give away the animal’s hiding spot. Within 20 to 40 ms of having revealed the prey’s location—before the prey can escape—the eel attacks it with a high-frequency discharge and immobilizes it for capture.

Figure A The electric eel Electrophorus electricus

Some strongly electric fish were known in ancient times. Aristotle described how the Mediterranean torpedo, which can deliver shocks of 50 to 60 V and several amperes of current, hides in wait to stun and then consume its prey. Francesco Redi (in 1671) and Stephano Lorenzini (in 1678) dissected torpedoes and concluded that the EO was derived from muscle. Nearly 300 years later, in the 1950s, fish with EOs that generate only weak electrical pulses were discovered in Africa and South America.

Combined observations of EOs in many unrelated fish indicate that EOs have evolved independently at least six different times. Recently, researchers have studied the genomic basis of the convergent evolution of EOs. Figure B illustrates the phylogeny of known groups of electric fish and identifies those used in a study of gene expression in EO tissues. The cellular morphology of EOs varied greatly among the animals studied (marked with asterisks), yet these divergent animals showed striking convergence in patterns of upregulation and downregulation of genes and transcription factors expressed to produce the physiological features of EOs.

Figure B Phylogeny of electric fishes This phylogenetic tree shows that electric organs evolved independently in six different orders of vertebrates. (After Gallant et al. 2014.)

Whereas genes involved in differentiation of muscle structures and functions are downregulated in all EOs, those involved in EO function are upregulated. For example, the genes for certain ion channels and transporters are highly expressed, which would contribute to increased excitability of the electrocytes. Certain collagen genes are also upregulated, presumably to produce the insulating connective tissue that prevents dissipation of the current produced by the electrocytes. Finally, the electric fish from divergent taxa all upregulated genes for insulin-like growth factors (IGFs), which turn on cellular mechanisms that contribute to large cell size. Thus, despite the widely varied morphologies of EO tissues in divergent fish, selection pressures appear to have exploited convergent use of gene expression patterns that yield the features of functional EOs.

In the process of studying the physiology of EOs and learning how electric fish use them in their native habitats, investigators have also made discoveries about convergent evolution, animal behavior, and cellular differentiation. Furthermore, because EOs yield abundant amounts of nearly pure excitable membranes, they provide tissues for ever-more-sophisticated studies of channels and membrane receptors. Finally, the large quantities of AChE in many EOs provide a plentiful source of enzyme for studies of anticholinesterases, which are of interest both to environmentalists (who find synthetic anticholinesterases in toxic wastes) and investigators seeking ways to prolong ACh signals at specific synapses. The structure and diverse functions of EOs are explored in Box Extension 20.1.

The structure of EOs

In different animals, EOs are derived from different muscle lineages, including tail muscles, muscles of the body axis, and oculomotor muscles (muscles that move the eyes). The electrocytes, like all other vertebrate skeletal muscle cells, are innervated by presynaptic cholinergic motor neurons, possess postsynaptic nicotinic ACh receptors, and use acetylcholinesterase (AChE) to hydrolyze ACh released upon stimulation. However, the flattened electrocytes (or electroplates) of EOs have few if any sarcomeres, do not contract, and are notably larger than muscle fibers (Figure C). The electocytes are stacked into columns; a single column may consist of thousands of electrocytes, and an EO—depending on the species of fish—can contain 50 to 1000 columns. Although the electrocytes do not contract, each responds to a neural signal by changing its membrane potential by some tens of millivolts. Because all of the electrocytes in a column respond to neural input simultaneously, their summed responses can produce large whole-animal voltage changes. The electric eel E. electricus (see Figure A) can produce electrical potentials of up to 600 V!

Figure C The electric eel Electrophorus electricus possesses both strong and weak electric organs (1) The strongly electric main organ and weakly electric Hunter’s and Sach’s organs form the bulk of the posterior mass of the animal. (2) A cross section reveals the electrocytes of several columns arranged on either side of the midline of the animal. Each column, which is separated by insulating tissue from adjacent columns, extends the length of the electric organ parallel with the long axis of the fish. Each electrocyte is shaped like a ribbon 4 cm long, 1.5 mm wide, and 100 μm thick. The posterior surface of each electrocyte receives a synapse (not shown) from a motor neuron extending from the spinal cord. (3) When the electrocyte is stimulated by a motor neuron, the membrane of the posterior innervated surface generates an action potential with a robust overshoot. The membrane potential across the noninnervated surface does not change. A change of 150 mV occurs across the electrocyte at the peak of the action potential. Because the electrocytes are arranged in series, their voltage changes are additive. A column containing 3000 electrocytes, for example, would generate 450 V. Columns of electrocytes are arranged in parallel. The more columns that are stimulated, the greater the total current flow. (Part 2 after Gotter et al. 1998. Part 3 after Stryer 1995, based on Keynes and Martins-Ferreira 1953.)

The diverse functions of EOs

In addition to possessing EOs that generate pulses of bioelectricity, most electric fish also have electroreceptors (see Chapter 14) that give them the ability to detect electric fields from external sources. The strongly electric species appear to use their electroreceptive capabilities to detect prey and potential predators. They use their EOs to stun prey and to ward off predators.

The weakly electric species use their EOs for electrolocation and communication. Many electric fish live in murky waters and are nocturnal. Electrolocation allows them to explore the environment without depending on vision. The EO generates constant discharges of a particular frequency that produce weak electric currents flowing out of the animal into the surrounding water. Nearby objects, which have electrical properties different from those of the water, alter the pattern of currents. These alterations are detected by electroreceptor organs in the skin of the animal, providing an “electric image.”

To communicate, weakly electric fish use discharges of their EOs to indicate the sending fish’s species, sex, and even individual identity. These signals are detected by the receiving fish’s electroreceptor organs. Ongoing studies show that EO signals can be modified by neuroendocrine stimuli influenced by social interactions and environmental conditions.

References

Gallant, J. R., and 15 additional authors. 2014. Genomic basis for the convergent evolution of electric organs. Science 344: 1522–1525.

Gotter, A. L., M. A. Kaetzel, and J. R. Dedman. 1998. Electrophorus electricus as a model system for the study of membrane excitability. Comp. Biochem. Physiol., A 119: 225–241.

Keynes, R. D., and H. Martins-Ferreira. 1953. Membrane potentials in the electroplates of the electric eel. J. Physiol. 119: 315–351.
(This classic paper describes the first use of intracellular microelectrodes to record the membrane potentials of the electroplates of Electrophorus electricus L.)

Stryer, Lubert. 1995. Biochemistry, 4th ed. W.H. Freeman and Company, New York, NY.