Abstract
Cognitive theories suggest that working memory maintains not only the identity of recently-presented stimuli but also a sense of the elapsed time since the stimuli were presented. Previous studies of the neural underpinnings of working memory have focused on sustained firing, which can account for maintenance of the stimulus identity, but not for representation of the elapsed time. We analyzed single-unit recordings from the lateral prefrontal cortex (lPFC) of two macaque monkeys during performance of a delayed-match-to-category task. Each sample stimulus triggered a consistent sequence of neurons, with each neuron in the sequence firing during a circumscribed period of time. These sequences of neurons encoded both stimulus identity and the elapsed time. The encoding of the elapsed time became less precise as the sample stimulus receded into the past. These findings suggest that working memory includes a compressed timeline of what happened when, consistent with longstanding cognitive theories of human memory.
Significance Statement Place cells in the hippocampus and other brain regions provide basis functions to support the dimension of physical space. Time cells, which activate sequentially provide analogous support for the dimension of time. We observed time cells in the macaque lPFC during a working memory task. The time cells we observed were stimulus specific meaning that they provide not only information about timing, but also conjunctively code what and when information. This representation thus constitutes a manifold with both temporal dimension and a stimulus-coding dimension that could support working memory. These temporal basis functions maintain a logarithmically-compressed timeline of the recent past, providing strong empirical support to long-standing cognitive theories of human memory.