Temporal processing in human memory

Qiaoli Huang, Jianrong Jia, Qiming Han, Huan Luo, Fast-backward replay of sequentially memorized items in humans, eLife 2018;7:e35164, DOI: 10.7554/eLife.35164.

Abstract

Storing temporal sequences of events (i.e., sequence memory) is fundamental to many cognitive functions. However, it is unknown how the sequence order information is maintained and represented in working memory and its behavioral significance, particularly in human subjects. We recorded electroencephalography (EEG) in combination with a temporal response function (TRF) method to dissociate item-specific neuronal reactivations. We demonstrate that serially remembered items are successively reactivated during memory retention. The sequential replay displays two interesting properties compared to the actual sequence. First, the item-by-item reactivation is compressed within a 200 – 400 ms window, suggesting that external events are associated within a plasticity-relevant window to facilitate memory consolidation. Second, the replay is in a temporally reversed order and is strongly related to the recency effect in behavior. This fast-backward replay, previously revealed in rat hippocampus and demonstrated here in human cortical activities, might constitute a general neural mechanism for sequence memory and learning.

eLife digest

Have you ever played the ‘Memory Maze Challenge’ game, or its predecessor from the 1980s, ‘Simon’? Players must memorize a sequence of colored lights, and then reproduce the sequence by tapping the colors on a pad. The sequence becomes longer with each trial, making the task more and more difficult. One wrong response and the game is over.

Storing and retrieving sequences is key to many cognitive processes, from following speech to hitting a tennis ball to recalling what you did last week. Such tasks require memorizing the order in which items occur as well as the items themselves. But how do we hold this information in memory? Huang et al. reveal the answer by using scalp electrodes to record the brain activity of healthy volunteers as they memorize and then recall a sequence.

Memorizing, or encoding, each of the items in the sequence triggered a distinct pattern of brain activity. As the volunteers held the sequence in memory, their brains replayed these activity patterns one after the other. But this replay showed two non-intuitive features. First, it was speeded up relative to the original encoding. In fact, the brain compressed the entire sequence into about 200 to 400 milliseconds. Second, the brain replayed the sequence backwards. The activity pattern corresponding to the last item was replayed first, while that corresponding to the first item was replayed last. This ‘fast-backward’ replay may explain why we tend to recall items at the end of a list better than those in the middle, a phenomenon known as the recency effect.

The results of Huang et al. suggest that when we hold a list of items in memory, the brain does not replay the list in its original form, like an echo. Instead, the brain restructures and reorganizes the list, compressing and reversing it. This process, which is also seen in rodents, helps the brain to incorporate the list of items into existing neuronal networks for memory storage.