Estrous hormones enhance coupled, rhythmic olivary discharge in correlation with facilitated limb stepping

Synchronized oscillatory behaviour of neurons within the dorsal accessory olive of the rat were monitored across spontaneous changes in rapid, co-ordinated limb movements associated with the estrous (hormone) and circadian cycles as well as following local administration of estradiol. Facilitation of rapid alterations in limb movement is observed following increases in circulating estradiol and progesterone on the night of behavioural estrus, as assessed by the ability of a rat to maintain a consistent position on a treadmill in response to variable changes in acceleration. Synchronized olivary activity was determined using chronically implanted bundles of microwires (50 μm diameter) to record from as many as 23 individual olivary neurons simultaneously across several four to five day estrous cycles, and in some cases after injection of the estrous hormones, estradiol and/or progesterone, either by systemic or local administration. Rats were tested during non-movement, constant speed locomotion or using a variable acceleration paradigm. Olivary oscillations were most commonly observed during treadmill locomotion with variable changes in acceleration. Local administration of estradiol, in combination with systemic progesterone administration, enhanced rhythmic olivary oscillations during this paradigm. At this time, at least a six-fold increase in the size of the coupled cluster of rhythmically discharging olivary neurons was observed compared with values obtained on diestrus, a low hormone state. Similar facilitating effects on olivary oscillations were observed on estrus, or following systemic injection of both estrous hormones. Administration of either steroid alone was not as effective. During the dark phase of the light:dark cycle, the oscillatory behaviour of these neurons was enhanced more than five-fold than during the light phase, and coupling diameter was maximal on the night of behavioural estrus. The synchronized oscillatory discharge of neurons within the olive is a putative timing mechanism which may underlie hormone-associated facilitation of rapid limb movements. The results from the present study provide evidence that both hormonal and circadian factors can enhance olivary rhythmicity in association with behavioural rhythmicity.