From Oscillators to Modulators: Behavioral and Neural Control of Modulations of the Electric Organ Discharge in the Gymnotiform Fish, Apteronotus Leptorhynchus

J Physiol Paris. Sep-Dec 2002;96(5-6):459-72. doi: 10.1016/S0928-4257(03)00002-0.

Abstract

The brown ghost (Apteronotus leptorhynchus) is a weakly electric gymnotiform fish that produces wave-like electric organ discharges distinguished by their enormous degree of regularity. Transient modulations of these discharges occur both spontaneously and when stimulating the fish with external electric signals that mimic encounters with a neighboring fish. Two prominent forms of modulations are chirps and gradual frequency rises. Chirps are complex frequency and amplitude modulations lasting between 20 ms and more than 200 ms. Based on their biophysical characteristics, they can be divided into four distinct categories. Gradual frequency rises consist of a rise in discharge frequency, followed by a slow return to baseline frequency. Although the modulatory phase may vary considerably between a few 100 ms and almost 100 s, there is no evidence for the existence of distinct categories of this type of modulation signal. Stimulation of the fish with external electric signals results almost exclusively in the generation of type-2 chirps. This effect is independent of the chirp type generated by the respective individual under non-evoked conditions. By contrast, no proper stimulation condition is known to evoke the other three types of chirps or gradual frequency rises in non-breeding fish. In contrast to the type-2 chirps evoked when subjecting the fish to external electric stimulation, the rate of spontaneously produced chirps is quite low. However, their rate appears to be optimized according to the probability of encountering a conspecific. As a result, the rate of non-evoked chirping is increased during the night when the fish exhibit high locomotor activity and in the time period following external electric stimulation. These, as well as other, observations demonstrate that both the type and rate of modulatory behavior are affected by a variety of behavioral conditions. This diversity at the behavioral level correlates with, and is likely to be causally linked to, the diversity of inputs received by the neurons that control chirps and gradual frequency rises, respectively. These neurons form two distinct sub-nuclei within the central posterior/prepacemaker nucleus in the dorsal thalamus. In vitro tract-tracing experiments have elucidated some of the connections of this complex with other brain regions. Direct input is received from the optic tectum. Indirect input arising from telencephalic and hypothalamic regions, as well as from the preoptic area, is relayed to the central posterior/prepacemaker nucleus via the preglomerular nucleus. Feedback loops may be provided by projections of the central posterior/prepacemaker nucleus to the preglomerular nucleus and the nucleus preopticus periventricularis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Behavior, Animal / physiology*
  • Biological Clocks / physiology*
  • Circadian Rhythm / physiology
  • Electric Organ / physiology*
  • Gymnotiformes / physiology*
  • Nerve Net / physiology*