Structure and function of neurons in the complex of the nucleus electrosensorius of Sternopygus and Eigenmannia: diencephalic substrates for the evolution of the jamming avoidance response.
The ability to discriminate the sign of the difference in frequency (DF) between two wavelike signals is integral to the jamming avoidance response (JAR) of weakly electric gymnotiform fish such as Eigenmannia. 'Whole-cell' intracellular recordings from neurons in the nucleus electrosensorius (nE) of Sternopygus, a gymnotiform that lacks the JAR, revealed that this nucleus receives information from both the ampullary and the tuberous electrosensory systems. Most tuberous units responded to DF stimuli, and many of these cells were DF sign-sensitive, i.e., they responded differently for one sign of DF. Although the distribution of ampullary units was somewhat restricted, sign-sensitive units were found in all areas of the nE in Sternopygus. Whole-cell recordings made in the nE of Eigenmannia revealed that, as in Sternopygus, sign-sensitive cells were not restricted to areas associated with control of the JAR. The diverse neurophysiology and connectivity of the nucleus electrosensorius suggests that, besides its role in the JAR of some members of the order, this nucleus likely serves as an interface between sensory input and neural circuits controlling other behaviors and endocrinological states in other gymnotiforms as well. The discovery of sign sensitivity in the nE of Sternopygus indicates that this property is not uniquely associated with the presence of a JAR; rather, the ability to discriminate the sign of DF may be relevant to many other behavioral contexts in gymnotiforms. Existing evidence indicates that the JAR evolved more than once in this group; the presence of sign sensitivity in ancestral gymnotiforms may have made this parallelism more likely.