Differential activation of glutamate receptor subtypes on a single class of cells enables a neural oscillator to produce distinct behaviors.

Electric fish generate different types of abrupt modulations of their electric organ discharge (EOD) rhythm to convey specific social signals. Intracellular recordings were made from neurons of the medullary pacemaker nucleus, which generates and transmits the rhythm that drives the EOD, to study the neuronal basis of two such modulations of the regular EOD rhythm, sudden accelerations, and abrupt interruptions. Recordings were both in vivo, and in a new in vitro brain preparation of Hypopomus pinnicaudatus (order Gymnotiformes). In vivo recordings during triggered behaviors indicated that abrupt modulations of the EOD rhythm are generated in the medullary pacemaker nucleus at the level of the relay cells, which are the projection cells of the nucleus, and not the pacemaker cells. In the in vitro brain stem preparation, cells of the pacemaker nucleus were spontaneously and rhythmically active as in the intact animal. Distinct modulations of the pacemaker nucleus rhythm that closely resembled those seen during natural behaviors could be triggered by electrical stimulation of afferent fibers. Modulations of the rhythm also could be triggered by direct pharmacological activation of the relay cells. When non-N-methyl-D-aspartate (NMDA) receptors were activated, relay cells were transiently depolarized and generated bursts of synchronized action potentials. NMDA receptor activation, alternatively, initiated a prolonged depolarization in the relay cells, during which time they failed to relay the regular pacemaker rhythm. The two firing states of the relay cell directly correlate with sudden accelerations and abrupt interruptions of the EOD.