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Acetylcholine Engages Distinct Amygdala Microcircuits to Gate Internal Theta Rhythm
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2024-04-24 , DOI: 10.1523/jneurosci.1568-23.2024
Joshua X. Bratsch-Prince , James W. Warren , Grace C. Jones , Alexander J. McDonald , David D. Mott

Acetylcholine (ACh) is released from basal forebrain cholinergic neurons in response to salient stimuli and engages brain states supporting attention and memory. These high ACh states are associated with theta oscillations, which synchronize neuronal ensembles. Theta oscillations in the basolateral amygdala (BLA) in both humans and rodents have been shown to underlie emotional memory, yet their mechanism remains unclear. Here, using brain slice electrophysiology in male and female mice, we show large ACh stimuli evoke prolonged theta oscillations in BLA local field potentials that depend upon M3 muscarinic receptor activation of cholecystokinin (CCK) interneurons (INs) without the need for external glutamate signaling. Somatostatin (SOM) INs inhibit CCK INs and are themselves inhibited by ACh, providing a functional SOM->CCK IN circuit connection gating BLA theta. Parvalbumin (PV) INs, which can drive BLA oscillations in baseline states, are not involved in the generation of ACh-induced theta, highlighting that ACh induces a cellular switch in the control of BLA oscillatory activity and establishes an internally BLA-driven theta oscillation through CCK INs. Theta activity is more readily evoked in BLA over the cortex or hippocampus, suggesting preferential activation of the BLA during high ACh states. These data reveal a SOM->CCK IN circuit in the BLA that gates internal theta oscillations and suggest a mechanism by which salient stimuli acting through ACh switch the BLA into a network state enabling emotional memory.



中文翻译:

乙酰胆碱参与独特的杏仁核微电路来控制内部 Theta 节律

乙酰胆碱 (ACh) 从基底前脑胆碱能神经元响应显着刺激而释放,并参与支持注意力和记忆的大脑状态。这些高 ACh 状态与 θ 振荡相关,从而使神经元群同步。人类和啮齿动物基底外侧杏仁核(BLA)的 Theta 振荡已被证明是情绪记忆的基础,但其机制仍不清楚。在这里,利用雄性和雌性小鼠的脑切片电生理学,我们发现大的 ACh 刺激会引起 BLA 局部场电位的延长的 θ 振荡,这取决于胆囊收缩素 (CCK) 中间神经元 (IN) 的 M3 毒蕈碱受体激活,而不需要外部谷氨酸信号传导。生长抑素 (SOM) IN 抑制 CCK IN,并且本身被 ACh 抑制,从而提供门控 BLA theta 的功能性 SOM->CCK IN 电路连接。小清蛋白 (PV) IN 可以在基线状态下驱动 BLA 振荡,但不参与 ACh 诱导的 theta 的生成,这强调了 ACh 诱导细胞开关控制 BLA 振荡活动,并建立内部 BLA 驱动的 theta 振荡通过 CCK IN。 BLA 中的 Theta 活性比皮质或海马体更容易被激发,这表明 BLA 在高 ACh 状态下优先激活。这些数据揭示了 BLA 中的 SOM->CCK IN 电路,该电路控制内部 θ 振荡,并提出了一种机制,通过 ACh 作用的显着刺激将 BLA 切换到支持情绪记忆的网络状态。

更新日期:2024-04-25
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