Department of Neurosurgery, Emory University, Atlanta, GA 30322.
Department of Psychology, Emory University, Atlanta, GA 30322.
Proc Natl Acad Sci U S A. 2018 Jan 2;115(1):98-103. doi: 10.1073/pnas.1714058114. Epub 2017 Dec 18.
Emotional events are often remembered better than neutral events, a benefit that many studies have hypothesized to depend on the amygdala's interactions with memory systems. These studies have indicated that the amygdala can modulate memory-consolidation processes in other brain regions such as the hippocampus and perirhinal cortex. Indeed, rodent studies have demonstrated that direct activation of the amygdala can enhance memory consolidation even during nonemotional events. However, the premise that the amygdala causally enhances declarative memory has not been directly tested in humans. Here we tested whether brief electrical stimulation to the amygdala could enhance declarative memory for specific images of neutral objects without eliciting a subjective emotional response. Fourteen epilepsy patients undergoing monitoring of seizures via intracranial depth electrodes viewed a series of neutral object images, half of which were immediately followed by brief, low-amplitude electrical stimulation to the amygdala. Amygdala stimulation elicited no subjective emotional response but led to reliably improved memory compared with control images when patients were given a recognition-memory test the next day. Neuronal oscillations in the amygdala, hippocampus, and perirhinal cortex during this next-day memory test indicated that a neural correlate of the memory enhancement was increased theta and gamma oscillatory interactions between these regions, consistent with the idea that the amygdala prioritizes consolidation by engaging other memory regions. These results show that the amygdala can initiate endogenous memory prioritization processes in the absence of emotional input, addressing a fundamental question and opening a path to future therapies.
情绪事件通常比中性事件更容易被记住,许多研究假设这种好处依赖于杏仁核与记忆系统的相互作用。这些研究表明,杏仁核可以调节海马体和边缘区等其他大脑区域的记忆巩固过程。事实上,啮齿动物研究表明,即使在非情绪事件中,杏仁核的直接激活也可以增强记忆巩固。然而,杏仁核因果增强陈述性记忆的前提尚未在人类中得到直接检验。在这里,我们测试了对杏仁核进行短暂的电刺激是否可以增强对中性物体特定图像的陈述性记忆,而不会引起主观的情绪反应。十四名癫痫患者通过颅内深部电极监测癫痫发作,观看了一系列中性物体图像,其中一半图像在观看后立即对杏仁核进行短暂的低幅度电刺激。杏仁核刺激不会引起主观的情绪反应,但与对照组图像相比,当患者第二天进行识别记忆测试时,记忆明显提高。在第二天的记忆测试中,杏仁核、海马体和边缘区的神经元振荡表明,记忆增强的神经相关物是这些区域之间增加的θ和γ振荡相互作用,这与杏仁核通过参与其他记忆区域来优先巩固的观点一致。这些结果表明,杏仁核可以在没有情绪输入的情况下启动内源性记忆优先化过程,解决了一个基本问题,并为未来的治疗方法开辟了道路。