Cellular characterization of synaptic modulations of a neuronal oscillator in electric fish

Abstract

The two closely related gymnotiform electric fish, Eigenmannia and Apteronotus, modulate the rate of their electric organ discharges during orientation and communication behaviors in similar ways. These modulations are controlled through three prepacemaker nuclei that provide excitatory inputs to the medullary pacemaker nucleus. Whereas the projections from the prepacemaker nuclei onto the two identified cell types of the pacemaker nucleus appear to be very similar, species-specific differences in the synaptic effects of these connections exist. We examined the modulatory premotor inputs on relay and pacemaker cells in Eigenmannia and Apteronotus by performing intracellular in␣vivo recordings while pharmacologically stimulating the three prepacemaker nuclei. In both taxa, activation of the lateral portion of the diencephalic prepacemaker causes a depolarization of baseline and a lowering of peak voltage primarily in relay cells. Activation of the medial portion of the diencephalic prepacemaker depolarizes mainly pacemaker cells in both fish, yet also has different effects on peak voltage in each species. Excitation of the sublemniscal prepacemaker in Apteronotus results in a depolarization of relay cells, whereas its inhibition in Eigenmannia causes a lowering of peak voltage without affecting baseline voltage. Our results complement earlier pharmacological investigations by expanding them to the cellular level. They provide neurophysiological evidence for different receptor subtypes on relay and pacemaker cells mediating different behaviors.