Glutamatergic Control Of A Pattern-Generating Central Nucleus In A Gymnotiform Fish

Abstract

The activity of pattern-generating networks (CPG) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. Gymnotus omarorum, a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. G. omarorum emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication. The EOD is considered the behavioral output of an electromotor CPG which, modulated by descending influences, organizes adaptive electromotor behaviors in response to environmental and social challenges. The CPG is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. We used electrophysiological and pharmacological techniques in brainstem slices of G. omarorum to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptors subtypes. We also show, for the first time in gymnotiformes, that glutamatergic control of the CPG likely involves both AMPA-NMDA receptors transmitting and only-NMDA segregated synapses contacting pacemaker cells. Our data shed light on the fast neurotransmitter control of a vertebrate CPG that seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. NEW & NOTEWORTHYUnderpinnings of neuromodulation of pattern-generating central networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involve the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.