Mauthner cell-initiated electromotor behavior is mediated via NMDA and metabotropic glutamatergic receptors on medullary pacemaker neurons in a gymnotid fish

Weakly electric fish generate meaningful electromotor behaviors by specific modulations of the discharge of their medullary pacemaker nucleus from whi ch the rhythmic command for each electric organ discharge (EOD) arises. Cer tain electromotor behaviors seem to involve the activation of specific neur otransmitter receptors on particular target cells within the nucleus, i.e., on pacemaker or on relay cells. This paper deals with the neural basis of the electromotor behavior elicited by activation of Mauthner cells in Gymno tus carapo. This behavior consists of an abrupt and prolonged increase in t he rate of the EOD. The effects of specific glutamate agonists and antagoni sts on basal EOD frequency and on EOD accelerations induced by Mauthner cel l activation were assessed. Injections of both ionotropic (AMPA, kainate, a nd NMDA) and metabotropic (trans-(+/-)-1-amino-1,3-cyclopentanedicarboxylic acid) glutamate agonists induced increases in EOD rate that were maximal w hen performed close to the soma of pacemaker cells. In contrast, injections in the proximity of relay cells were ineffective. Therefore, pacemaker neu rons are probably endowed with diverse glutamate receptor subtypes, whereas relay cells are probably not. The Mauthner cell-evoked electromotor behavi or was suppressed by injections of AP-5 and (+/-)-amino-4-carboxy-methyl-ph enylacetic acid, NMDA receptor and metabotropic glutamate receptor antagoni sts, respectively. Thus, this electromotor behavior relies on the activatio n of the NMDA and metabotropic glutamate receptor subtypes of pacemaker cel ls. Our study gives evidence for the synergistic effects of NMDA and metabo tropic receptor activation and shows how a simple circuit can produce speci fic electromotor outputs.