Functional synchronization between hippocampal sEEG, parietal ECoG and scalp EEG during a verbal working memory task.

Abstract

BackgroundThe maintenance of items in working memory (WM) relies on a widespread network of brain areas where synchronization between electrophysiological recordings may reflect functional coupling. While the coupling from hippocampus to scalp EEG is well established, we provide here direct cortical recordings for a fine-grained analysis. MethodsA patient performed a WM task where a string of letters was presented all at once, thus separating the encoding period from the maintenance period. We recorded sEEG from the hippocampus, temporo-parietal ECoG from a 64-contact grid electrode, and scalp EEG. ResultsPower spectral density (PSD) showed a clear task dependence: PSD in the posterior parietal lobe (10 Hz) and in the hippocampus (20 Hz) peaked towards the end of the maintenance period. Inter-area synchronization was characterized by the phase locking value (PLV). WM maintenance enhanced PLV between hippocampal sEEG and scalp EEG specifically in the theta range [6 7] Hz. PLV from hippocampus to parietal cortex increased during maintenance in the [9 10] Hz alpha and the 20 Hz range. When analyzing the information flow to and from auditory cortex by Granger causality, the flow was from auditory cortex to hippocampus with a peak in the [8 18] Hz range while letters were presented, and this flow was subsequently reversed during maintenance, while letters were maintained in memory. ConclusionsThe increased functional interaction between hippocampus and cortex through synchronized oscillatory activity and the directed information flow provide physiological basis for reverberation of memory items during maintenance. This points to a network for working memory that is bound by coherent oscillations involving cortical areas and hippocampus. SIGNIFICANCE STATEMENTHippocampal activity is known for its role in cognitive tasks involving episodic memory or spatial navigation, but its role in working memory and its sensitivity to workload is still under debate. Here, we investigated hippocampal and cortical activity while a subject maintained sets of letters in verbal working memory for a few seconds to guide action. After confirming the coupling between hippocampal oscillations and oscillations on the scalp, we found during maintenance that hippocampal oscillations increased coupling differentially to several areas of cortex by recording directly from the cortex.. During encoding of the letters, information flow was from auditory cortex to hippocampus and subsequently reversed during maintenance, thus providing a physiological basis for memory encoding and maintenance. This demonstrates a network for working memory that is bound by coherent oscillations that underlie the functional connectivity between cortical areas and hippocampus.