Rhythmic temporal coordination of neural activity avoids representational conflict during working memory

Abstract

Selective attention1 is characterized by alternating states associated with either attentional sampling or attentional shifting, helping to avoid functional conflicts by isolating function-specific neural activity in time2-5. We hypothesized that such rhythmic temporal coordination might also help to avoid representational conflicts during working memory6. Multiple items can be simultaneously held in working memory, and these items can be represented by overlapping neural populations7-9. Traditional theories propose that short-term storage of to-be-remembered items occurs through persistent neural activity10-12, but when neurons are simultaneously representing multiple items, persistent activity creates a potential for representational conflicts. In comparison, more recent, activity-silent theories of working memory propose that synaptic changes also contribute to the short-term storage of to-be-remembered items13-16. Transient bursts in neural activity17, rather than persistent activity, could serve to occasionally refresh these synaptic changes. Here, we used EEG and response times (RTs) to test whether rhythmic temporal coordination helps to isolate neural activity associated with different to-be-remembered items, which would help to avoid representational conflicts. Consistent with this hypothesis, we report that the relative strength of different item representations alternates over time as a function of frequency-specific phase. Although RTs were linked to theta (~6Hz) and beta (~25 Hz) phase during a memory delay, the relative strength of item representations only alternated as a function of beta phase. The present findings (i) are consistent with rhythmic temporal coordination being a general mechanism for avoiding either functional or representational conflicts during cognitive processes, and (ii) inform models describing the role of oscillatory dynamics in organizing working memory13,18-21.