Stimulation of the Posterior Cortical-Hippocampal Network Enhances Precision of Memory Recollection

Abstract

Summary Episodic memory is thought to critically depend on interaction of the hippocampus with distributed brain regions [1–3]. Specific contributions of distinct networks have been hypothesized, with the hippocampal posterior-medial (HPM) network implicated in recollection of highly precise contextual and spatial information [3–6]. Current evidence for HPM specialization is mostly indirect, derived from correlative measures such as neural activity recordings. Here, we tested the causal role of HPM in recollection using network-targeted noninvasive brain stimulation in humans, which has previously been shown to increase functional connectivity within the HPM network [7]. Effects of multiple-day electromagnetic stimulation were assessed using an object-location memory task that segregated recollection precision from general recollection success. HPM network-targeted stimulation produced lasting (~24 h) enhancement of recollection precision, without effects on general success. Canonical neural correlates of recollection [8–10] were also modulated by stimulation. Late-positive evoked potential amplitude and theta-alpha oscillatory power were reduced, suggesting that stimulation can improve memory through enhanced reactivation of detailed visuospatial information at retrieval. The HPM network was thus specifically implicated in processing of fine-grained memory detail, supporting functional specialization of hippocampal-cortical networks. These findings demonstrate that brain networks can be causally linked to distinct and specific neurocognitive functions and suggest mechanisms for long-lasting changes in memory due to network-targeted stimulation.

Episodic memory improvements due to noninvasive stimulation targeting the cortical–hippocampal network: A replication and extension experiment

“…Furthermore, the current findings do not support the proposal that increased episodic learning due to stimulation comes at the price of accelerated long‐term forgetting. Considered with other conceptual replications (Hermiller et al, ; Kim et al, ; Nilakantan et al, , ; Tambini et al, ), the current results support the notion that noninvasive stimulation targeting the hippocampal–cortical network can influence recollective memory tasks that are widely considered hippocampal‐dependent.…”

“…The current experiment also sought to address potential mechanisms whereby network-targeted stimulation improves memory. The effects of network-targeted stimulation on memory demonstrated in previous experiments (Kim et al, 2018;Nilakantan et al, 2017Nilakantan et al, , 2019Tambini et al, 2018;Wang & Voss, 2015) have been improvements in new learning ability. In these studies, the memory assessment involved learning a novel set of memoranda and then taking the memory test after a relatively brief delay (minutes to hours) on the same day.…”

“…The effects of stimulation on the targeted hippocampal–cortical network have been measured using memory testing and neuroimaging. There have been several demonstrations of improved recollection memory performance (Kim et al, ; Nilakantan et al, , ; Tambini et al, ; Wang et al, ) as well as corresponding changes in neuroimaging‐based measures of network function (Hermiller et al, ; Kim et al, ; Nilakantan et al, ; Wang et al, ). These experiments have therefore been important for identifying the role of hippocampal–cortical networks in memory.…”

“…These previous experiments have used different episodic memory outcomes, including cued recall of face‐word associates (Wang et al, ), spatial reconstruction (Nilakantan et al, ; Tambini et al, ), and paired‐associate recognition (Kim et al, ; Nilakantan et al, ). Findings that stimulation improved performance for these various test formats, all of which measure hippocampal‐dependent recollection, provide important conceptual replications of the phenomenon of improved episodic memory due to stimulation targeting the hippocampal–cortical network.…”

“…The distributed network of the human hippocampus includes regions such as the medial prefrontal, medial parietal, and lateral parietal cortex and is thought to support episodic memory (Buckner, Andrews-Hanna, & Schacter, 2008;Mesulam, 1990;Ranganath & Ritchey, 2012). Several experiments have tested contributions of the hippocampal-cortical network to memory using noninvasive brain stimulation (Hermiller, VanHaerents, Raij, & Voss, 2019;Kim et al, 2018;Nilakantan, Bridge, Gagnon, VanHaerents, & Voss, 2017;Nilakantan et al, 2019;Tambini, Nee, & D'Esposito, 2018;Wang et al, 2014). These experiments have used a network targeting approach, whereby transcranial magnetic stimulation (TMS) was applied to cortical regions defined based on their resting-state fMRI connectivity with the hippocampus.…”