Dependence of Working Memory on Coordinated Activity Across Brain Areas

Abstract

Neural signatures of working memory (WM) have been reported in numerous brain areas, suggesting a distributed neural substrate for memory maintenance. In the current manuscript we provide an updated review of the literature focusing on intracranial neurophysiological recordings during WM in primates. Such signatures of WM include changes in firing rate or local oscillatory power within an area, along with measures of coordinated activity between areas based on synchronization between oscillations. In comparing the ability of various neural signatures in any brain area to predict behavioral performance, we observe that synchrony between areas is more frequently and robustly correlated with WM performance than any of the within-area neural signatures. We further review the evidence for alteration of inter-areal synchrony in brain disorders, consistent with an important role for such synchrony during behavior. Additionally, results of causal studies indicate that manipulating synchrony across areas is especially effective at influencing WM task performance. Each of these lines of research supports the critical role of inter-areal synchrony in WM. Finally, we propose a framework for interactions between prefrontal and sensory areas during WM, incorporating a range of experimental findings and offering an explanation for the observed link between intra-areal measures and WM performance.

Information flows from hippocampus to auditory cortex during replay of verbal working memory items

“…PLV in the [4][5][6][7][8] Hz theta range increased significantly with several contacts over auditory cortex (permutation test p<0.05, Fig 2 g). This speaks for a functional coupling between auditory cortex and hippocampus mediated by synchronized oscillations [26].…”

“…In cortical brain regions, WM maintenance correlates with sustained neuronal oscillations, most frequently reported in the theta-alpha range (4-12 Hz) [3-7, 9-20] or at even lower frequencies [25, 26]. Also in the hippocampus, WM maintenance was associated with sustained theta-alpha oscillations [15, 19].…”

Effective connectivity of working memory performance: a DCM study of MEG data

“…Neural activity supporting working memory (WM) is distributed throughout the brain (Christophel et al, 2017 ; Sreenivasan and D'Esposito, 2019 ; Mejías and Wang, 2022 ), motivating the view that WM may be better understood as a distributed network function, rather than being localized to specific brain regions (Lorenc and Sreenivasan, 2021 ; Rezayat et al, 2022 ), as suggested by evidence of task-dependent reorganization of large-scale brain networks during WM (e.g., Cohen and D'Esposito, 2016 ). This “new” perspective of WM was anticipated by Patricia Goldman-Rakic, who pioneer the study of the neurobiological underpinnings of WM (Goldman-Rakic, 1995 ).…”

Brain-wide human oscillatory LFP activity during visual working memory

“…In recent years, analysis of intracranial recordings from human subjects have provided evidence for existence of persistent spiking activity during the maintenance of working memory (Kaminski et al, 2017) and other properties of human brain activation during working memory (Haller et al, 2018; Gehrig et al, 2019; Kumar et al, 2021; Xie et al, 2023). Analysis of non-human primate recordings has also begun to mirror methods of analysis inspired by human studies (Rezayat et al, 2021). However differences in behavioral paradigms and methods of analyses persist and make comparison of findings from different models challenging.…”

“…Analysis of non-human primate recordings has also begun to mirror methods of analysis inspired by human studies (Rezayat et al, 2021). However differences in behavioral paradigms and methods of analyses persist and make comparison of findings from different models challenging.…”