Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval

Episodic memory is thought to arise as a function of dynamic interactions between the hippocampus and the neocortex, yet the mechanisms by which these interactions manifest have remained elusive. Here, using human intracranial recordings during a mnemonic discrimination task, we report that 4-5 Hz (overlapping with theta) power is differentially recruited during pattern separation compared to overgeneralization errors, and its phase supports interactions between the hippocampus and the neocortex when memories are being formed and correctly retrieved. Interactions were largely bidirectional, with small but significant net directional biases; a hippocampus-to-neocortex bias during the acquisition of new information that was subsequently correctly discriminated from similar stimuli, and a neocortex-to-hippocampus bias during the accurate discrimination of new stimuli from similar previously learned stimuli at retrieval. These results may be somewhat surprising given predictions from Complementary Learning Systems and similar models and provide new insights into the mechanisms by which the two learning systems (hippocampus and neocortex) may support episodic memory. The 4-5 Hz rhythm may facilitate the initial stages of information acquisition by neocortex during learning (i.e., hippocampus  neocortex information transfer) and the recall of stored information from cortex during retrieval (i.e., neocortex  hippocampus information transfer), in the context of a discrimination memory task. Future work should further probe these dynamics across different types of tasks and stimuli and computational models may need to be expanded accordingly to accommodate these findings.

篇章记忆被认为起源于海马体与新皮层之间动态交互的作用，然而这些交互作用的具体机制仍显晦涩难解。本研究通过在记忆辨别任务期间对人类颅内进行记录，报告指出，在模式分离过程中，4-5赫兹（与θ波重叠）的功率相较于泛化错误，存在差异性的招募，其相位支持海马体与新皮层在记忆形成和正确提取过程中的交互作用。这些交互作用大体呈双向性，存在微小但显著的净方向偏差；在海马体向新皮层传输新信息并随后正确辨别相似刺激的过程中，表现出海马体向新皮层的偏差；在回忆过程中，新刺激与先前学习过的相似刺激的正确辨别中，表现出新皮层向海马体的偏差。这些结果可能与互补学习系统及类似模型的预测有所出入，并为两个学习系统（海马体与新皮层）如何支持篇章记忆的机制提供了新的见解。4-5赫兹的节律可能在学习初期阶段促进新皮层的信息获取（即，海马体→新皮层的信息传递）以及在学习过程中从皮层提取存储的信息（即，新皮层→海马体的信息传递），这在辨别记忆任务背景下尤为明显。未来的研究应进一步探究不同类型任务和刺激下的这些动态变化，相应的，计算模型可能需要相应地扩展以适应这些发现。