Modulation of Oscillatory Power and Connectivity in the Human Posterior Cingulate Cortex Supports the Encoding and Retrieval of Episodic Memories

Abstract

Existing data from noninvasive studies have led researchers to posit that the posterior cingulate cortex (PCC) supports mnemonic processes: It exhibits degeneration in memory disorders, and fMRI investigations have demonstrated memory-related activation principally during the retrieval of memory items. Despite these data, the role of the PCC in episodic memory has received only limited treatment using the spatial and temporal precision of intracranial EEG, with previous analyses focused on item retrieval. Using data gathered from 21 human participants who underwent stereo-EEG for seizure localization, we characterized oscillatory patterns in the PCC during the encoding and retrieval of episodic memories. We identified a subsequent memory effect during item encoding characterized by increased gamma band oscillatory power and a low-frequency power desynchronization. Fourteen participants had stereotactic electrodes located simultaneously in the hippocampus and PCC, and with these unique data, we describe connectivity changes between these structures that predict successful item encoding and that precede item retrieval. Oscillatory power during retrieval matched the pattern we observed during encoding, with low-frequency (below 15 Hz) desynchronization and a gamma band (especially high gamma, 70-180 Hz) power increase. Encoding is characterized by synchrony between the hippocampus and PCC, centered at 3 Hz, consistent with other observations of properties of this oscillation akin to those for rodent theta activity. We discuss our findings in light of existing theories of episodic memory processing, including the information via desynchronization hypothesis and retrieved context theory, and examine how our data fit with existing theories for the functional role of the PCC. These include a postulated role for the PCC in modulating internally directed attention and for representing or integrating contextual information for memory items.

Stimulation of the posterior cingulate impairs episodic memory encoding

“…Positive t--values correspond to an increase in power in ES versus NS conditions. Specifically, we found that hippocampal power decreased in theta band (2--10 Hz) but increased in low gamma (25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40) and high gamma bands (>40Hz) in the ES compared to NS condition across all participants ( Fig. 3b).…”

“…Electrode Localization. Localization of electrodes was performed by pre--surgical planning followed by stereotactic placement of depth electrodes and postoperative fusion of CT images with the pre--operative high--resolution MRI Images (MPRAGE, coronally acquired 1 mm slices) as conducted in our prior studies (40,61). Depth electrodes were labeled using Freesurfer's auto--segmentation software (http://surfer.nmr.mgh.harvard.edu/) (62).…”

“…We reasoned that if neural activation in the PCC predominantly reduces during successful memory encoding (20--24), then high frequency stimulation delivered to the PCC during encoding might enhance memory. To test our hypothesis, we applied stimulation using robotically placed stereotactic electroencephalography (stereo EEG) electrodes implanted for seizure mapping, based on our prior work (40). This unique technique allows: (i) precise targeting of deep brain regions such as the PCC (Fig.…”

Frequency‐specific noninvasive modulation of memory retrieval and its relationship with hippocampal network connectivity

“…HCN interregional interactions important for memory have been particularly associated with activity synchrony in the theta-frequency band. For instance, human intracranial recordings have shown that HCN regions exhibit neuronal synchrony and phase locking at thetaband frequencies (4-8-Hz) at rest (Foster & Parvizi, 2012), during memory formation (Lega, Jacobs, & Kahana, 2012;Rutishauser, Ross, Mamelak, & Schuman, 2010) and during memory retrieval (Anderson, Rajagovindan, Ghacibeh, Meador, & Ding, 2010;Burke et al, 2014;Foster, Kaveh, Dastjerdi, Miller, & Parvizi, 2013;Lega, Germi, & Rugg, 2017;Steinvorth, Wang, Ulbert, Schomer, & Halgren, 2010;Watrous, Tandon, Conner, Pieters, & Ekstrom, 2013). Likewise, invasive electrical theta-burst stimulation, whereby gamma bursts are applied in a theta cycle ("theta nested gamma"), preferentially induces long-term potentiation in the rodent hippocampus (Larson, Wong, & Lynch, 1986), putatively because this stimulation pattern mimics the endogenous activity of the hippocampus (Buzsaki, 2002).…”

Neural correlates of exceptional memory ability in SuperAgers: A multimodal approach using FDG-PET, PIB-PET, and MRI

“…The Default Mode Network (DMN), typically associated with memory system and self-thoughts, has been demonstrated to be affected by age-related cognitive decline, thus presenting reduced FC between the anterior cingulate and posterior cingulate in older individuals (Dennis and Thompson, 2014;Koch et al, 2010). Previous studies have highlighted the pivotal role of cingulate regions in successful memory encoding (Grady et al, 2003;Lee et al, 2016) and retrieval (Lega et al, 2017). Nonetheless, it is not possible to completely evaluate the complexity of human cognitive processes using a single method of analysis.…”