Significance of Findings on Electroreception for General Neurobiology

Summary

Electroreceptors and their central pathways belong to the octavolateral system and offer many contrasts and similarities to lateral line, auditory, and vestibular reception. Some of the contrasts are based on the presumption that electroreception involves no mechanical steps in transduction, whereas the other octavolateral modalities are mechanical but may involve an electrical step in transduction. The finding that electroreceptors work as voltmeters and govern transmitter release by small changes in membrane potential raises a question that goes beyond these closely related modalities: Is it possible that some other sensory or central cells also come under the influence of weak extracellular fields? Among the phenomena of general neurobiological interest that are particularly obvious or accessible in electric sense cells are ultrastructural changes in ribbon synapses with activity; tight junctions around sense cells far from their equator, causing asymmetrical voltage drops across apical and basal membranes; loss of stereocilia and variations in kinocilia; absence of centrifugal nerve fibers to the sense cells; resonance of receptors at their best excitatory frequency—and the plastic alteration of such individual tuning, in development and with hormones; a variety of receptor types in respect to the way the afferent axon encodes stimulus parameters; and lifelong addition of sense cells to a presumably fixed number of afferent axons.

Central representation and processing provide examples of four parallel body maps in the first-order medullary nucleus converging on a single laminar stack of congruent maps in the midbrain nucleus equivalent to the inferior colliculus; computed maps of the best dipole axis; parallel pathways for different submodalities; and various schemes for dealing with reafference, with and without corollary discharges, some central expectations being plastic. Electrical sensing offers instructive evidence of convergence giving improved resolution, larger and more complex receptive fields, direction specificity, and best distance units; central filtering added to peripheral tuning; different amplitude modulation (AM) best frequencies that may shift with modulation depth; and an increased adaptation rate in medullary nuclei due to descending projections. One form of normal social behavior, the jamming avoidance response, is rather fully understood through some 14 orders of neurons, from receptor to effector, and illustrates a distributed, "parliamentary," high-precision mechanism.

Brain regions with equivalents in other vertebrates that have yielded particularly rich details, anatomically or physiologically, include the primary nuclei in the octavolateral medulla, torus semicircularis, tectum, and cerebellum. Each is specialized in some species, often elaborately.

Sensorimotor integration is illuminated by favorable preparations for examining parameters of response control. Electroreception includes the active mode in which electric signals are generated by the animal's own electric organ discharges (EODs), and it includes communication by modulation of EODs; therefore this volume includes some aspects of the diverse forms of electric organs and their control. High-precision biological clocks and their fine modulation; the use of electrical and chemical synapses; devices for synchronization; and extreme specialization of Ranvier nodes are among the adaptations of general interest. Regeneration of the spinal cord extends to reconstitution of the cellular detail.

Ethological comparisons among the species in respect to electroreception touch upon orientation, object location, communication, and other uses. Ecological comparisons raise general questions such as those regarding the sources of signals and noise. Evolutionary comparisons reveal a wealth of detail on convergent development of effector and receptor organs, central pathways, and physiological and behavioral adaptations.