Stimulus discrimination in the diencephalon of Eigenmannia: the emergence and sharpening of a sensory filter

Abstract

Neuronal reliability and sensitivity to behaviorally relevant stimulus patterns were investigated in a higher-order nucleus of the diencephalon believed to participate in the jamming avoidance response (JAR) of the weakly electric fish, Eigenmannia. The fish raises or lowers its frequency of electric organ discharge (EOD) to minimize interference from a neighboring fish's EOD. Proper JARs require determination of the sign of the difference frequency (Df) between the neighboring fish's EOD and the fish's own EOD. Bastian and Yuthas (1984) recently described diencephalic neurons within the nucleus electrosensorius that are able to make this determination. In the present study, response properties of such neurons were compared with those of lower-level 'sign-selective' cells found in the torus semicircularis and the optic tectum (Heiligenberg and Rose 1985) as well as with properties of the intact behavior. Most sign-selective cells within the nucleus electrosensorius show a high degree of selectivity for one sign of the difference frequency; cells with either sign preference were found in approximately equal numbers. The sign preference and the degree of sign selectivity is most often independent of the spatial orientation of the jamming stimulus. In contrast, the responses of toral and tectal cells are less robust and consistent and are often highly dependent on the geometry of the jamming stimulus. Determination of the sign of the difference frequency requires the analysis of amplitude modulations coupled with modulations in phase (timing) differences between pairs of areas of the body surface. The most sensitive cells recorded in the nucleus electrosensorius can determine the sign of the difference frequency with timing differences of 1 microsecond or less, roughly comparable to the behavioral threshold of 400 ns (Carr et al. 1986). The best toral/tectal response required at least a 16 microseconds modulation. Cells within the nucleus electrosensorius thus code the sign of Df with a high degree of reliability and sensitivity. Ambiguities persist, however, which suggest that single cells at this level cannot completely account for the behavioral discrimination. Additional processing may be necessary to transform a still primarily sensory code into a motor program for control of the JAR (Rose et al. 1988).