The estrous cycle and the olivo-cerebellar circuit. I. Contrast enhancement of sensorimotor-correlated cerebellar discharge.

The estrous cycle and the olivo-cerebellar circuit. I. Contrast enhancement of sensorimotor-correlated cerebellar discharge.
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发情周期和橄榄小脑回路。

DOI:
10.1007/bf00228726
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发表时间:
1996
影响因子:
2
通讯作者:
Chapin,JK
Chapin,JK
中科院分区:
医学4区
文献类型:
--
作者:
Smith,SS;Chapin,JK

文献摘要

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单胺和发情激素对浦肯野(Pnj)细胞反应的神经调节在小脑的细胞水平上得到了很好的表征,但在清醒行为动物的神经元回路水平上却没有。在本研究中,通过长期植入微丝电极束,获得了橄榄-小脑回路内多达16个单个神经元的同时记录:在恒定或变速的跑步机运动任务中,记录了3-20个连续的发情期,同时记录了小脑皮层旁Pnj细胞样神经元(Pnj cln)及其攀爬纤维输入传入源吻侧背侧副橄榄(rDAO)神经元的排列。在跑步机运动中记录的超过90%的pnjcln在站立运动阶段表现出显著的活动增加(80%)或减少(10%)。相比之下,来自rDAO的细胞在速度变化或大鼠无法保持跑步机速度(位置滑移)时增加了活性。在由循环17β-雌二醇和孕酮水平升高引发的行为性发情夜,与姿态相关的pnjcln活性的升高和降低幅度均增加了85-115%。这些结果与我们之前的研究结果一致,17β-雌二醇和孕酮分别增强了单个Pnj细胞对局部谷氨酸和GABA的兴奋和抑制反应。这种兴奋和抑制作用的双重增强,在细胞水平上显然是矛盾的,在神经元集合水平上产生了神经种群“信号”对比的显著增强。此外,pnjcln在发情期间的姿态相关放电比发情期间提前约120ms。逐帧视频分析还表明,发情时与退情(低激素状态)相比,阶梯周期的摆动阶段缩短。此外,与行为发情夜相比,与速度变化或体位滑移相关的rDAO放电也显著增加(P<0.05)。因此,发情与pnjcln的振幅和时间变化有关,rDAO放电与特定行为事件相关。这些与发情相关的Pnj细胞活性变化与对跑步机速度随机变化的更快反应(r= 0.84)有很好的相关性(r= 0.84)。综上所述,这些研究结果表明,在性类固醇激素循环水平达到峰值后观察到的与站立相关的Phj - cln放电对比的增加与在随机移动的跑步机上运动表现的改善有关。
Neuromodulation of Purkinje (Pnj) cell responses by monoamines and estrous hormones is well characterized in the cerebellum at the cellular level, but not at the level of neuronal circuits in the awake behaving animal. In the present study, simultaneous recordings of up to 16 single neurons from within the olivo-cerebellar circuit were obtained through chronically implanted microwire electrode bundles: arrays of Pnj cell like neurons (Pnj cln) in the paravermal cerebellum and neurons within the afferent source of its climbing fiber input, the rostral dorsal accessory olive (rDAO), were recorded simultaneously across 3–20 consecutive estrous cycles during constant or variable speed treadmill locomotion performance tasks. Over 90% of Pnj cln recorded during treadmill locomotion exhibited significant increases (80%) or decreases (10%) in activity correlated with the stance phase of locomotion. In contrast, cells from the rDAO increased activity during speed changes or when the rat failed to maintain the treadmill speed (position slip). On the night of behavioral estrus, which is triggered by elevations in circulating levels of 17β-estradiol and progesterone, the magnitude of both increases and decreases in stance-correlated Pnj cln activity increased by 85–115%. These results are consistent with our previous findings that 17β-estradiol and progesterone enhance excitatory and inhibitory responses of single Pnj cells to locally applied glutamate and GABA, respectively. This dual enhancement of both excitatory and inhibitory effects, apparently paradoxical at the cellular level, produced a marked heightening of thecontrastof the neural population “signal” at the neuronal ensemble level. Furthermore, the stance-correlated discharge of Pnj cln during estrus preceded that during diestrus by ∼120ms. Frame-by-frame video analysis also suggested that the swing phase of the step cycle was shortened on estrus compared with diestrus (low hormone state). In addition, rDAO discharge correlated with speed change or position slip was also significantly increased (P<0.05) on the night of behavioral estrus versus diestrus. Thus, estrus was associated with changes in both the amplitude and the timing of Pnj cln and rDAO discharge correlated with specific behavioral events. These estrous-associated changes in Pnj cell activity were well correlated (r= 0.84) with faster responses to random changes in treadmill speed, a motor performance task. Together, these findings suggest that the increases in the contrast of stancecorrelated Phj cln discharge observed following peak circulating levels of sex steroid hormones are associated with improved motor performance on a randomly moving treadmill.