Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates

Abstract

The two closely related gymnotiform fishes, Apteronotus and Eigenmannia, share many similar communication and electrolocation behaviors that require modulation of the frequency of their electric organ discharges. The premotor linkages between their electrosensory system and their medullary pacemaker nucleus, which controls the repetition rate of their electric organ discharges, appear to function differently, however. In the context of the jamming avoidance response, Eigenmannia can raise or lower its electric organ discharge frequency from its resting level. A normally quiescent input from the diencephalic pre-pacemaker nucleus can be recruited to raise the electric organ discharge frequency above the resting level. Another normally active input, from the sublemniscal pre-pacemaker nucleus, can be inhibited to lower the electric organ discharge frequency below the resting level (Metzner 1993). In contrast, during a jamming avoidance response, Apteronotus cannot lower its electric organ discharge frequency below the resting level. The sublemniscal pre-pacemaker is normally completely inhibited and release of this inhibition allows the electric organ discharge frequency to rise during the jamming avoidance response. Further inhibition of this nucleus cannot lower the electric organ discharge frequency below the resting level. Lesions of the diencephalic pre-pacemaker do not affect performance of the jamming avoidance response. Thus, in Apteronotus, the sublemniscal pre-pacemaker alone controls the changes of the electric organ discharge frequency during the jamming avoidance response.

Dynamics of jamming avoidance in echolocating bats

“…perforatus) exhibits such a JAR. We also demonstrate that the JAR in individual T. teniotis consists of both symmetric static and asymmetric dynamic components, which differ from JAR in wave species of weakly electric fishes, where either symmetric or asymmetric JAR occurs in a given species (Heiligenberg et al 1996).…”

“…Some wave species of electric fishes (Eigenmannidae) show symmetric JAR, increasing their discharge frequencies in response to low-frequency signals and decreasing their frequencies in response to high-frequency signals. Other wave species (Apteronotidae) show asymmetric JAR, increasing their discharge frequencies only in response to interfering signals (Heiligenberg et al 1996). The symmetry or asymmetry of the JAR is a characteristic of fish species, and is served by functionally different neural circuitry (Heiligenberg 1977;Metzner 1999).…”

“…JAR in pulse species involves changes in interpulse intervals (IPIs) minimizing temporal coincidences between pulses of neighbouring conspecifics; JAR in wave species involves changes in discharge frequency, minimizing spectral overlap between frequencies of neighbouring conspecifics (Heiligenberg 1977(Heiligenberg , 1991Kawasaki 1997;Metzner 1999). In electric fishes, JAR is supported by neural circuits that were extensively characterized in several species (Scheich 1977;Carr et al 1986;Heiligenberg 1991;Heiligenberg et al 1996;Metzner 1999), and it enhances individual electrolocation performance (Heiligenberg 1991), and possibly also social identification and communication among individuals (Kramer 1999).…”

Evolution and hormonal regulation of sex differences in the electrocommunication behavior of ghost knifefishes (Apteronotidae)

“…An alternative possibility is that the PPn-C might control only low-frequency chirps, and that high-frequency chirps might be regulated by the sublemniscal prepacemaker nucleus (SPPn), a midbrain nucleus that also provides glutamatergic excitation to relay neurons in the PMN and that mediates the jamming avoidance response. Strong electrical stimulation of the SPPn produces interruption-like modulations of the EOD with large frequency increases and amplitude decreases that resemble high-frequency chirps (Heiligenberg et al, 1996).…”

The energetics of electric organ discharge generation in gymnotiform weakly electric fish

“…Pacemaker neurons and relay neurons are electrotonically coupled via gap junctions supporting synchronous firing among all PN neurons (Moortgat et al, 2000a). The activity of the PN is under the control of two prepacemaker nuclei, the sublemniscal prepacemaker nucleus (SPPN) and the prepacemaker nucleus (PPN), whose input can gradually or rapidly accelerate EOD frequency and, in some species, decelerate EOD frequency or even cause cessation of EO firing (Heiligenberg et al, 1981;Heiligenberg et al, 1996;Kawasaki and Heiligenberg, 1989;Keller et al, 1991;Metzner, 1993;Metzner, 1999).…”