Guth Tim A, Brandt Armin, Reinacher Peter C, Schulze-Bonhage Andreas, Jacobs Joshua, Kunz Lukas
Department of Epileptology, University Hospital Bonn, Bonn, Germany.
Epilepsy Center, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
bioRxiv. 2024 Jun 20:2024.06.20.599841. doi: 10.1101/2024.06.20.599841.
The precise timing of single-neuron activity in relation to local field potentials may support various cognitive functions. Extensive research in rodents, along with some evidence in humans, suggests that single-neuron activity at specific phases of theta oscillations plays a crucial role in memory processes. Our fundamental understanding of such theta-phase locking in humans and its dependency on basic electrophysiological properties of the local field potential is still limited, however. Here, using single-neuron recordings in epilepsy patients performing a spatial memory task, we thus aimed at improving our understanding of factors modulating theta-phase locking in the human brain. Combining a generalized-phase approach for frequency-adaptive theta-phase estimation with time-resolved spectral parameterization, our results show that theta-phase locking is a strong and prevalent phenomenon across human medial temporal lobe regions, both during spatial memory encoding and retrieval. Neuronal theta-phase locking increased during periods of elevated theta power, when clear theta oscillations were present, and when aperiodic activity exhibited steeper slopes. Theta-phase locking was similarly strong during successful and unsuccessful memory, and most neurons activated at similar theta phases between encoding and retrieval. Some neurons changed their preferred theta phases between encoding and retrieval, in line with the idea that different memory processes are separated within the theta cycle. Together, these results help disentangle how different properties of local field potentials and memory states influence theta-phase locking of human single neurons. This contributes to a better understanding of how interactions between single neurons and local field potentials may support human spatial memory.
单个神经元活动相对于局部场电位的精确时间可能支持各种认知功能。对啮齿动物的广泛研究以及一些人类研究证据表明，θ振荡特定阶段的单个神经元活动在记忆过程中起着关键作用。然而，我们对人类这种θ相位锁定及其对局部场电位基本电生理特性的依赖性的基本理解仍然有限。在此，我们利用癫痫患者在执行空间记忆任务时的单神经元记录，旨在增进我们对调节人类大脑中θ相位锁定因素的理解。将用于频率自适应θ相位估计的广义相位方法与时间分辨谱参数化相结合，我们的结果表明，θ相位锁定在空间记忆编码和检索过程中，是人类内侧颞叶区域普遍存在的强烈现象。在θ功率升高、出现清晰的θ振荡以及非周期性活动呈现更陡斜率的时期，神经元的θ相位锁定增加。在成功和不成功的记忆过程中，θ相位锁定同样强烈，并且大多数神经元在编码和检索之间的相似θ相位处被激活。一些神经元在编码和检索之间改变了它们偏好的θ相位，这与不同记忆过程在θ周期内分离的观点一致。总之，这些结果有助于理清局部场电位的不同特性和记忆状态如何影响人类单个神经元的θ相位锁定。这有助于更好地理解单个神经元与局部场电位之间的相互作用如何支持人类空间记忆。
