Central control of electric signaling behavior in the mormyrid Brienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition

Abstract

SUMMARY Like all mormyrid fish, Brienomyrus brachyistius produces an electric organ discharge (EOD) with a constant waveform and variable sequence of pulse intervals (SPI). Periodic bursts fall into two display categories termed `scallops' and `accelerations', with a third category termed `rasps'that appears to combine the two. The medullary EOD command nucleus (CN)receives excitatory input from the midbrain precommand nucleus (PCN) and the thalamic dorsal posterior nucleus (DP), both of which are regulated by a recurrent inhibitory projection from the ventroposterior nucleus of the torus semicircularis (VP). We tested the following hypotheses: (1) PCN and DP are responsible for generating different burst types (scallops and accelerations,respectively), (2) differences in the strength of recurrent inhibition are related to physiological differences between PCN and DP and (3) recurrent inhibition regulates the resting electromotor rhythm, while disinhibition releases PCN and DP, allowing them to generate bursts. Iontophoresis of the excitatory neurotransmitter l-glutamate (l-Glu) into DP led to acceleration-like output patterns, while in PCN it led to scallop-like output patterns. Iontophoresis of the inhibitory neurotransmitterγ-amino-butyric acid (GABA) into DP and PCN led to an elongation of intervals, as did iontophoresis of l-Glu into VP. Iontophoresis of the GABAA receptor blocker bicuculline methiodide (BMI) into DP and PCN induced repetitive bursting behavior and eliminated differences in the effects of l-Glu iontophoresis in the two nuclei. These results support our three hypotheses, suggesting that production of different communication behaviors may be regulated by spatially distinct groups of neurons, and recurrent inhibition and disinhibition may play an active role in driving and shaping such behaviors.