Opposing actions of androgen and estrogen on in vitro firing frequency of neuronal oscillators in the electromotor system

Abstract

The South American knifefish (Apteronotus leptorhynchus), or brown ghost, produces a high-frequency (600-1000 Hz) sinusoidal electric organ discharge (EOD) with males discharging at higher frequencies than females. In addition, each fish has a unique EOD frequency within the frequency range of its gender. The electromotor circuit responsible for EOD production consists of a medullary pacemaker nucleus (PMN) and spinal electromotor neurons (EMNs). In vitro spinal slice recording showed that, similar to the PMN, EMNs fire spontaneously at rates near the EOD frequency of each fish. The persistence of firing 2 weeks after high spinal transection demonstrated that spontaneous firing rate was intrinsic to the EMNs and was not dependent on presynaptic input. We confirmed that 11-ketotestosterone (11 kT) raised and 17-β-estradiol (E2) lowered the EOD frequency of intact fish. Because electromotor cells fire spontaneously near EOD frequency, we investigated whether these steroids affect endogenous firing rates. Steroid implants were made in normal or spinally transected fish. Two weeks later, PMNs of normal fish and EMNs of transected fish were recorded in vitro. 11 kT increased and E2 decreased the intrinsic firing rate of neurons in the PMN and the EMNs. Hormones shifted the intrinsic firing rates of EMNs, although they were synaptically isolated during the hormone exposure.