Decoding working memory information from neurons with and without persistent activity in the primate prefrontal cortex.

Abstract

Persistent activity of neurons in the prefrontal cortex has been thought to represent the information maintained in working memory, though alternative models have challenged this idea. Theories that depend on the dynamic representation of information posit that stimulus information may be maintained by the activity pattern of neurons whose firing rate is not significantly elevated above their baseline during the delay period of working memory tasks. We thus tested the ability of neurons that do and do not generate persistent activity in the prefrontal cortex of monkeys to represent spatial and object information in working memory. Neurons that generated persistent activity represented more information about the stimuli in both spatial and object working memory tasks. The amount of information that could be decoded from neural activity depended on the choice of decoder and parameters used but neurons with persistent activity outperformed non-persistent neurons consistently. Averaged across all neurons and stimuli, the firing rate did not appear clearly elevated above baseline during the maintenance of neural activity particularly for object working memory; however, this grand average masked neurons that generated persistent activity selective for their preferred stimuli, which carried the majority of stimulus information. These results reveal that prefrontal neurons that generate persistent activity maintain information more reliably during working memory.NEW & NOTEWORTHY Competing theories suggest that neurons that generate persistent activity or do not are primarily responsible for the maintenance of information, particularly regarding object working memory. Although the two models have been debated on theoretical terms, direct comparison of empirical results has been lacking. Analysis of neural activity in a large database of prefrontal recordings revealed that neurons that generate persistent activity were primarily responsible for the maintenance of both spatial and object working memory.