Intermediate Physics for Medicine and Biology: Electroreception

Friday, November 5, 2021

Electroreception

Suppose you’re reading Homework Problem 4 in Chapter 8 of Intermediate Physics for Medicine and Biology, and you run across the phrase “If a shark can detect an electric field strength of 0.5 μV m⁻¹…”. What’s your first reaction? Probably you suspect a typo (it isn’t). An electric field with a strength of 0.5 μV m⁻¹ is tiny. By comparison, you need a field of about 10 V m⁻¹ to stimulate a neuron in the brain. How can a shark detect a field of only 0.0000005 V m⁻¹? The answer makes for an interesting story.

Some of the first studies of electroreception—the ability of some animals, such as sharks, to sense weak electric fields—were performed by a biophysicist at Woods Hole Oceanographic Institute named Adrianus Kalmijn. He observed dogfish sharks while sitting in an inflatable rubber raft in the ten-foot deep water of the Atlantic Ocean near Martha’s Vineyard. Kalmijn attracted the sharks using liquified herring placed on the ocean floor. On either side of the herring was a pair of electrodes that could be used to pass current. The dogfish were initially attracted by the smell of the herring, and “began frantically searching over the sand, apparently trying to locate the odor source” (Kalmijn, 1977). But when current was turned on, the dogfish stopped searching for the herring and “viciously attacked” the electrodes! Using experiments like these, Kalmijn was able to characterize how sharks respond to electric fields.

Spiny dogfish (Squalus acanthias) at the Josephine Marie shipwreck, Stellwagen National Marine Laboratory. From Wikipedia.

Sharks detect weak electric fields using sensory organs called the ampullae of Lorenzini. The ampullae consist of highly conducting jelly-filled tubes about 30 cm long (a little more than a foot). The shark detects the voltage across the length of the tube, and then places that entire voltage difference across a single cell membrane. An electric field of 0.5 μV m⁻¹ multiplied by a distance of 0.3 m gives you a voltage of 0.15 μV. There’s an extra factor of three arising from the distortion of the field by the shark, so you end up with a transmembrane voltage of about half a microvolt.

A membrane voltage of 0.5 μV is minuscule. The typical resting membrane voltage of a cell is approximately 70 mV, so half a microvolt is less than ten parts per million. How can such a small voltage change be detected? To answer this question, William Pickard, an engineer at Washington University in St. Louis, assumed that this membrane voltage does not cause a neuron to fire (it’s far too weak for that), but instead modulates its spontaneous firing rate. The neuron normally operates in a regime where this rate is very sensitive to the membrane voltage, which has the effect of magnifying a small change in voltage into a large change in rate (Pickard, 1988).

Many ampullae of Lorenzini influence a single neuron. Their summation has the effect of averaging out any background noise. The size of thermal voltage fluctuations across a neuron’s membrane were estimated by Yale physicist Robert Adair to be about 1 μV (Adair, 1991), which is twice as large as the membrane voltage produced by the smallest electric field a shark can detect. Integrating the signal over hundreds of ampullae suppresses these fluctuations, allowing the system to pick a signal out of the thermal background. This sensory mechanism has been honed by evolution to be about as sensitive as it can be without detecting the constant roar of random noise.