The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways.

Abstract

The gymnotiform fish Eigenmannia generates weakly electric signals for electrolocation and communication. The signals are produced by electric organ discharges (EODs) that are driven by a medullary pacemaker nucleus. To avoid jamming by neighboring conspecifics with similar frequencies, a fish raises its own EOD frequency if the neighbor's frequency is lower, and it lowers its EOD frequency if the neighbor's frequency is higher (Watanabe and Takeda, 1963). Both the raising and lowering of EOD frequency of this jamming avoidance response (JAR; Bullock et al., 1972) are thought to be controlled by feature-extracting neurons in the diencephalic prepacemaker nucleus (PPn-G) that discriminate the sign of the frequency difference between the jamming signal and the fish's EOD (Kawasaki et al., 1988a; Rose et al., 1988; for review, see Heiligenberg, 1991). These prepacemaker neurons are excited in response to lower jamming frequencies, thereby raising the frequency, and inhibited by higher jamming frequencies, producing a discharge deceleration. The results of experiments presented here, however, suggest a mechanism for the motor control of the JAR that is different from the one described previously (see, e.g., Heiligenberg, 1991). Two prepacemaker nuclei, one PPn-G and one sublemniscal prepacemaker nucleus (SPPn) (Keller et al., 1991 a,b), which provide the only known inputs to the pacemaker, were lesioned selectively. This article explores the effects of these lesions on the JAR. Pharmacological experiments were used to elucidate the transmitter types involved. The results suggest that the JAR is controlled by two separate motor pathways. One controls frequency rises and originates in the dorsal substructure of the nucleus electrosensorius (Keller, 1988). It sends excitatory connections to the diencephalic prepacemaker and finally to the pacemaker nucleus, where AMPA-type receptors mediate the synaptic transmission. The second pathway controls frequency decreases and originates in the ventral substructure of the nucleus electrosensorius. It provides GABAergic input to the SPPn. The SPPn is tonically active and also controls the EOD frequency even in the absence of jamming signals. Its projection to the pacemaker nucleus is mediated by NMDA-type receptors. The results of this study suggest that there is no single population of final, feature-extracting elements or "recognition units" that controls JAR-related shifts of the pacemaker frequency. Instead, the motor control of the JAR consists of an interaction of two independent pathways according to a "push-pull" principle.