Estrogen-Dependent and Estrogen-Independent Effects of Progesterone on the Electrophysiological Excitability of Dorsal Midbrain Neurons in Golden Hamsters

Abstract

During the induction of lordosis responses in golden hamsters, the joint actions of estradiol (E) and progesterone (P) have been found to produce major changes in the activity levels, sensory responsiveness and movement-related firing of neurons in the dorsal midbrain, a region vital for lordosis in this species. The present study investigated the possibility that these effects of E and P on dorsal midbrain neurons might arise through changes in transsynaptic excitability or spike-generating processes. Single dorsal midbrain neurons were orthodromically or antidromically activated by ventromedial midbrain tegmental stimulation in ovariectomized, urethane-anesthetized hamsters before and after subcutaneous injection of P in propylene glycol vehicle. P injection produced two neurophysiological effects: (1) a strong depression of transsynaptic activation, and (2) in antidromically invaded neurons, a change in the amplitude (either an increase or decrease) of the soma-dendritic spike component. Both of these effects appeared rapidly (i.e. within 10–20 min) after P injection. The P effect on orthodromic neuronal excitability was contingent upon E priming of the hamsters, but, in contrast, the P effect on antidromic spike amplitude was not. Several features of these neurophysiological effects of P imply that the hormone may have been acting through nongenomic mechanisms, possibly involving receptors in neuronal membranes.

Rapid Neurophysiological Effects of Corticosterone on Medullary Neurons: Relationship to Stress-Induced Suppression of Courtship Clasping in an Amphibian

“…The reticulospi nal neurons sampled in this study were distinguished by the fact that they tended not to show spontaneous or sen sory stimulus-elicited discharges under the conditions of these experiments. This characteristic of brainstem neu rons with long, descending axons has been previously re ported in cats [ 19] and golden hamsters [ 17] and probably reflects a tendency of such neurons to fire only under re stricted circumstances, such as specific movement or pos tural conditions [20]. It was clear in the present study that the reticulospinal neurons as well as the active, responsive neurons, received synaptic inputs from similar afferent sources, particularly the cloaca and that sensory effects on antidromic spikes were also modified by CORT injection.…”

“…Stimulus intensities sufficient for antidromic activation of reticulo spinal neurons were usually less than 300 uA, except following CORT administration, as described in the Results. Antidromic acti vation of reticulospinal neurons by spinal cord stimulation was de termined according to the following standard criteria [15][16][17]: (1) short latency, single spike discharges; (2) a constant spike latency at threshold stimulation intensity; (3) well-defined threshold; (4) abil ity to follow paired pulses with short interpulse intervals (i.e. a re fractory period of approximately the duration of the action poten tial), and (5) evidence of an inflection on the initial phase of the action potential that was exaggerated at short interstimulus intervals and was sometimes accompanied by prolonged delay or absence of the somadendritic spike component.…”

Progesterone Signaling Mechanisms in Brain and Behavior

“…P signaling mediated by G protein βγ subunits have been shown to activate the downstream MAPK cascade during meiotic progression in Xenopus oocytes, demonstrating a biologically important role for G proteins in non-classical signaling (Blackmore, 1998; Ferrell and Machleder, 1998; Ferrell, 1999; Lutz et al, 2000). Rapid effects of steroid hormones have also been demonstrated on the release of LHRH (Ramirez et al, 1990), dopamine and acetylcholine (Meiri, 1986), release of excitatory amino acids (Smith et al, 1987), and changes in neuronal activity (Kelly et al, 1977a,b; Havens and Rose, 1988). In addition to P, several of its ring-A reduced metabolites have been shown to facilitate lordosis response in ovariectomized, E 2 -primed female rats via activation of MAPK pathway (Gonzalez-Flores et al, 2004, 2009).…”

Activation of progestin receptors in female reproductive behavior: Interactions with neurotransmitters

“…Rapid effects of P have been demonstrated in the release of gonadotropin releasing hormone (GnRH) [211], DA and acetylcholine [182] and excitatory amino acids [243], changes in neuronal activity [120, 136–137] and on facilitation of lordosis response in estrogen-primed female rats [142, 152, 181]. These rapid effects of P are not blocked by protein synthesis inhibitors, are mediated by their binding to putative cell surface membrane receptors [221–222], receptors that gate ion channels [94, 176], and are also coupled to certain second messenger systems [137, 147, 235].…”