Combined Phase-Rate Coding by Persistently Active Neurons as a Mechanism for Maintaining Multiple Items in Working Memory in Humans

Maintaining multiple items in working memory (WM) is central to human behavior. Persistently active neurons are thought to be a mechanism to maintain WMs, but it remains unclear how such activity is coordinated when multiple items are kept in memory. We show that memoranda-selective persistently active neurons in the human medial temporal lobe phase lock to ongoing slow-frequency (1-7 Hz) oscillations during WM maintenance. The properties of phase locking are dependent on memory content and load. During high memory loads, the phase of the oscillatory activity to which neurons phase lock provides information about memory content not available in the firing rate of the neurons. We provide a computational model that reveals that inhibitory-feedback-mediated competition between multiple persistently active neurons reproduces this phenomenon. This work reveals a mechanism for the active maintenance of multiple items in WM that relies on persistently active neurons whose activation is orchestrated by oscillatory activity.