Transduction at electroreceptors: origins of sensitivity

Electroreceptors of four different classes were analyzed in terms of adaptations leading to high sensitivity. The large receptor of mormyrids is a sensitive phasic receptor. Voltage amplification is provided by an impulse-generating mechanism in the receptor cells. The cells are specialized in that their threshold is very close to the resting potential. Inward current may be mediated by Ca channels, which show little inactivation. Transmission to the afferent nerve is electrotonic and is apparently not otherwise specialized. Other phasic receptors appear to use regenerative responsiveness more for active filtering than for voltage gain. Tonic electroreceptors of freshwater fishes lack regenerative responses in their receptor cells. Stimuli act directly on the presynaptic membrane to alter Ca permeability and modulate the release of transmitter. The absence of regeneration is ascribable to shunting by fixed conductances. The relation between transmitter release and depolarization is much steeper than the corresponding relation at the squid giant synapse. Indirect arguments suggest that the great voltage sensitivity does not reside in any properties of the Ca channels, but in subsequent processes leading to transmitter release. The ampulla of Lorenzini is the most sensitive electroreceptor. Its sensitivity apparently resides in the regenerative oscillatory activity of the receptor cells. The receptor is kept in its operating range by accommodative processes, probably involving Ca-activated outward current. A number of mechanisms of electroreception appear relevant to mechanosensitive acoustico-lateralis receptors. The specialized accommodative processes and the adaptations increasing sensitivity are likely to be relevant to many other systems as well.