Abstract
How does the human brain rapidly process incoming information in working memory? In growing divergence from a single-region focus on the prefrontal cortex (PFC), recent work argues for emphasis on how distributed neural networks are rapidly coordinated in support of this central neurocognitive function. Previously, we showed that working memory for everyday “what,” “where,” and “when” associations depends on multiplexed oscillatory systems, in which signals of different frequencies simultaneously link the PFC to parieto-occipital and medial temporal regions, pointing to a complex web of sub-second, bidirectional interactions. Here, we used direct brain recordings to delineate the frontoparietal oscillatory correlates of working memory with high spatiotemporal precision. Seven intracranial patients with electrodes simultaneously localized to prefrontal and parietal cortices performed a visuospatial working memory task that operationalizes the types of identity and spatiotemporal information we encounter every day. First, task-induced oscillations in the same delta-theta (2–7 Hz) and alpha-beta (9–24 Hz) frequency ranges previously identified using scalp electroencephalography (EEG) carried information about the contents of working memory. Second, maintenance was linked to directional connectivity from the parietal cortex to the PFC. However, presentation of the test prompt to cue identity, spatial, or temporal information changed delta-theta coordination from a unidirectional, parietal-led system to a bidirectional, frontoparietal system. Third, the processing of spatiotemporal information was more bidirectional in the delta-theta range than was the processing of identity information, where alpha-beta connectivity did not exhibit sensitivity to the contents of working memory. These findings implicate a bidirectional delta-theta mechanism for frontoparietal control over the contents of working memory.
Highlights
The ability to maintain and manipulate information in working memory provides the neurobiological infrastructure for thinking and complex cognition
We observed that the epoch corresponding to the selection of spatial information ended ∼50 ms before the start of the epoch corresponding to that of temporal information [shaded in blue]. These results suggest that working memory for spatial and temporal information is supported by relatively more prefrontal cortex (PFC)-led network interactions than for identity information, and that spatial and temporal information selection occurs serially in the delta-theta band
Using an ecologically valid task of working memory for everyday ‘‘what,’’ ‘‘where,’’ and ‘‘when’’ associations (Johnson et al, 2017, 2018), we show that oscillations between 2 Hz and 24 Hz displayed sensitivity to both within- and between-trial shifts in task demands
Summary
The ability to maintain and manipulate information in working memory provides the neurobiological infrastructure for thinking and complex cognition. Parallel alpha-beta (9–24 Hz) rhythms were observed in the parieto-occipital → PFC direction, and were neither responsive to shifts in task demands nor affected by PFC lesions, revealing an oscillatory response that was independent of the PFC These findings challenge dominant models of working memory which attribute function to PFC-dependent systems (Goldman-Rakic, 1995; Miller and Cohen, 2001; Curtis and D’Esposito, 2003; Müller and Knight, 2006; Lara and Wallis, 2014; Sreenivasan et al, 2014; Szczepanski and Knight, 2014; D’Esposito and Postle, 2015; Eriksson et al, 2015), and instead support a model of network-wide frontoparietal control (Wager and Smith, 2003; Duncan, 2010, 2013; Niendam et al, 2012; Cole et al, 2013; Ester et al, 2015, 2016; Sadaghiani and Kleinschmidt, 2016; Christophel et al, 2017)
Sign-in/Register to view highlights & summary 
Published Version (
Free)
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call