The hippocampus is a locus of working memory (WM) with anterior and posterior subregions that differ in their transcriptional and external connectivity patterns. However, the involvement and functional connections between these subregions in WM processing are poorly understood. To address these issues, we recorded intracranial EEG from the anterior and the posterior hippocampi in humans (seven females and seven males) who maintained a set of letters in their WM. We found that WM maintenance was accompanied by elevated low-frequency activity in both the anterior and posterior hippocampus and by increased theta/alpha band (3-12 Hz) phase synchronization between anterior and posterior subregions. Cross-frequency and Granger prediction analyses consistently showed that the correct WM trials were associated with theta/alpha band-coordinated unidirectional influence from the posterior to the anterior hippocampus. In contrast, WM errors were associated with bidirectional interactions between the anterior and posterior hippocampus. These findings imply that theta/alpha band synchrony within the hippocampus may support successful WM via a posterior to anterior influence. A combination of intracranial recording and a fine-grained atlas may be of value in understanding the neural mechanisms of WM processing.SIGNIFICANCE STATEMENT Working memory (WM) is crucial to everyday functioning. The hippocampus has been proposed to be a subcortical node involved in WM processes. Previous studies have suggested that the anterior and posterior hippocampi differ in their external connectivity patterns and gene expression. However, it remains unknown whether and how human hippocampal subregions are recruited and coordinated during WM tasks. Here, by recording intracranial electroencephalography simultaneously from both hippocampal subregions, we found enhanced power in both areas and increased phase synchronization between them. Furthermore, correct WM trials were associated with a unidirectional influence from the posterior to the anterior hippocampus, whereas error trials were correlated with bidirectional interactions. These findings indicate a long-axis specialization in the human hippocampus during WM processing.
Both the hippocampus and amygdala are involved in working memory (WM) processing. However, their specific role in WM is still an open question. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task, and compared their representation patterns during the encoding and maintenance periods. By combining multivariate representational analysis and connectivity analyses with machine learning methods, our results revealed a functional specialization of the amygdala-hippocampal circuit: The mnemonic representations in the amygdala were highly distinct and decreased from encoding to maintenance. The hippocampal representations, however, were more similar across different items but remained stable in the absence of the stimulus. WM encoding and maintenance were associated with bidirectional information flow between the amygdala and the hippocampus in low-frequency bands (1–40 Hz). Furthermore, the decoding accuracy on WM load was higher by using representational features in the amygdala during encoding and in the hippocampus during maintenance, and by using information flow from the amygdala during encoding and that from the hippocampus during maintenance, respectively. Taken together, our study reveals that WM processing is associated with functional specialization and interaction within the amygdala-hippocampus circuit.
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