Synaptic modulation of a neuronal oscillator: Segregation of cellular components within the pacemaker nucleus mediates different behaviors in electric fish

The pacemaker nucleus in gymnotiform fish is a neuronal oscillator unmatched in its regularity among biological systems. During the jamming avoidance response (JAR) and communication behavior in Eigenmannia, the rate of oscillation is stereotypically modulated by three separate synaptic inputs which converge at the level of the pacemaker nucleus. Both abrupt frequency accelerations associated with communication behavior and gradual frequency accelerations associated with the JAR are mediated by glutamatergic inputs from separate diencephalic nuclei. Based on previous results from pharmacological and immunohistochemical investigations, each behavior results from differential activation of AMPA and NMDA receptor subtypes, respectively, at the level of the pacemaker nucleus. In contrast, gradual frequency decelerations associated with the JAR are believed to be controlled by reducing tonic glutamatergic input from a mesencephalic nucleus onto NMDA receptors in the pacemaker nucleus. The interactions between these three extrinsic sources of synaptic input and the two cellular components of the neuronal oscillator, pacemaker and relay cells, is the subject of this dissertation. While recording intracellularly from pacemaker and relay cells in vivo, the activity of presynaptic inputs were selectively manipulated pharmacologically to elicit characteristic frequency modulations. Modifications in spike parameters were always cell-type specific. Furthermore, each of the three premotor inputs to the Pn modified the cellular responses of their target cells in a unique fashion. In order to explore this issue further, changes in input resistance were monitored in pacemaker and relay cells while pharmacologically manipulating the activity of each premotor synaptic input. During rapid frequency accelerations elicited by PPnC stimulation, a large, transient decrease in input resistance was observed primarily in relay cells. In contrast, during gradual EOD accelerations elicited by PPnG stimulation, a large sustained decrease in input resistance was observed primarily in pacemaker cells. Interestingly, gradual EOD decelerations elicited by SPPn inhibition resulted in an increase in input resistance primarily in relay cells. This finding is consistent with a cellular mechanism by which a tonic excitatory input is "turned off". Complementing our earlier qualitative investigations, these results provide direct quantitative evidence for the segregation of cellular and synaptic components within an oscillatory network mediating different behaviors.