Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval

Abstract

The medial temporal lobes, prefrontal cortex, and parts of parietal cortex form the neural underpinnings of episodic memory, which includes remembering both where and when an event occurred. Yet how these three key regions interact during retrieval of spatial and temporal context remains largely untested. Here, we employed simultaneous electrocorticographical recordings across multiple lobular regions, employing phase synchronization as a measure of network functional connectivity, while patients retrieved spatial and temporal context associated with an episode. Successful memory retrieval was characterized by greater global connectivity compared to incorrect retrieval, with the MTL acting as a convergence hub for these interactions. Spatial vs. temporal context retrieval resulted in prominent differences in both the spectral and temporal patterns of network interactions. These results emphasize dynamic network interactions as central to episodic memory retrieval, providing novel insight into how multiple contexts underlying a single event can be recreated within the same network.

Place Cells, Grid Cells, and Memory

“…Remarkably, the place cells responsive to the area where the item was delivered became active during recall of the item, closely mirroring the reactivation of place cells during replay events in rodents. Although free recall in humans is not likely to correspond to sharp-wave ripple events (Watrous et al 2013), the time course of reactivation was similar to a typical sharp-wave ripple event in rodents, and may therefore reflect a qualitatively similar phenomenon. The place cell activity during recall of events or items likely brings to mind the spatial context in which the events and items were experienced, creating a fully reconstructed memory for what was experienced, along with where it was experienced.…”

A network approach for modulating memory processes via direct and indirect brain stimulation: Toward a causal approach for the neural basis of memory

“…In addition to the relationship between increased coherence within specific frequency bands and better memory performance reported in some studies (Benchenane et al 2010;Fell et al, 2008;Watrous et al 2013), animal studies also have shown that direct electrical stimulation can entrain action potentials (i.e., spikes) and oscillatory activity (Anastassiou, Perin, Markram, & Koch, 2011;Fröhlich & McCormick, 2010). Thus, while the exact mechanisms whereby coordinated low-frequency oscillations between indirectly connected brain areas facilitate network function and behavior more broadly remain to be fully elucidated, macrostimulation that modulates synaptic and/or spiking activity in the targeted neuronal populations may be a promising approach to modulating oscillatory dynamics and function of a network.…”

“…Indeed, past neuroimaging studies have argued that lateral frontal and parietal regions are part of the core networks associated with memory encoding (Blumenfeld & Ranganath, 2007;Nyberg et al, 1996;Tulving et al, 1994) and/or retrieval (Cabeza et al, 2004;Cabeza et al, 2003Cabeza et al, , 2002Donaldson et al, 2001;Nyberg et al, 1996;Tulving et al, 1994;Vilberg & Rugg, 2008). More recent theoretical and empirical studies have argued that these regions are part of a larger network of interacting brain regions subserving memory (King, de Chastelaine, Elward, Wang, & Rugg, 2015;Schedlbauer, Copara, Watrous, & Ekstrom, 2014;Watrous et al, 2013). Thus, a key prediction is that disruption of extra-hippocampal nodes should also produce impairments in memory function.…”

“…Declarative memory relies on a distributed network of multiple neocortical and medial temporal regions that serve cohesive roles in memory processes (Battaglia, Benchenane, Sirota, Pennartz, & Wiener, 2011;Buzsáki, 1996;Eichenbaum, 2000;McClelland et al, 1995;Norman & O'Reilly, 2003;Preston & Eichenbaum, 2013;Watrous et al 2013). For example, functional connectivity, characterized by phase synchronization of oscillatory activity, between the medial temporal, frontal, and parietal regions is critical for successful memory retrieval (Watrous et al, 2013). Thus, it seems reasonable to suggest that stimulation will likely be more effective when it targets multiple brain areas in the functional networks rather than a single area in isolation.…”

“…For example, the hippocampus has direct projections with parahippocampal regions (Eichenbaum, 2000;Suzuki, 1996), and most of (Backus, Schoffelen, Szebényi, Hanslmayr, & Doeller, 2015;Benchenane et al, 2010;Buschman & Miller, 2007;Varela, Lachaux, Rodriguez, & Martinerie, 2001;Watrous et al, 23 2013;Womelsdorf et al, 2007). Moreover, increased coherence between brain regions, particularly hippocampus and prefrontal cortex, relates to better memory performance (Benchenane et al 2010;Fell, Ludowig, Rosburg, Axmacher, & Elger, 2008;Watrous et al 2013). Thus, coherent activity within specific frequency bands, reflected via the local field potential (LFP), may be an important way in which disparate brain areas exchange information.…”