Virtual Taxi Drivers: Network Interactions Underlying Memory Retrieval

Boone, C; Anderson, WS

doi: 10.1227/01.neu.0000438335.51481.13
Science Times

Review of: Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 2013 doi:10.1038/nn.3315.

Humans depend on a memory system to rapidly and veraciously store the massive stream of incoming information documenting their experiences, and faithfully represent and recall that information for future use. Devastating dysfunction in the system is observed in schizophrenia and Alzheimer’s disease. While the medial temporal lobe (MTL), prefrontal cortex (PFC), and parietal lobe have been implicated in an episodic memory retrieval network, the processes underlying successful retrieval remain undetermined, particularly regarding simultaneous recall of different classes of information represented by shared neuronal ensembles. Leading hypotheses propose that retrieval may be defined by changes in connectivity and activity of one region in the network, connections throughout the network, or phase-synchronized activity at specific frequencies. In a recent study, Watrous et al. tested these theories with simultaneous electrocortigraphical (ECoG) recordings from these regions during episodic memory retrieval.

Six patients with medically intractable epilepsy underwent invasive monitoring, and the derived data were used for this study. Electrodes were localized to subregions of the MTL, PFC, and parietal cortex. Patients performed a spatiotemporal memory-dependent task with a virtual taxi game, in which they drove passengers to five irregularly spaced stores in a specific sequential order. Once patients reached criteria levels of accuracy or training time, retrieval of spatial and temporal information was tested separately. Phase synchronization was utilized as a measure of functional connectivity to test the different hypotheses. Pairwise phase consistency (PPC) index, which is based on phase angle difference between signals from different electrodes, was used to quantify the phase synchronization across electrode pairs. Two subregions, termed nodes within the network, were considered functionally connected when the PPC between them differed significantly depending on the condition (correct vs. incorrect responses, spatial vs. temporal memory retrieval). The node degree, a node’s total number of connections, also marked the magnitude of connectivity. Nodes with the highest node degree were defined as hubs. With the greatest connectivity, a hub is thought to play a central role in mediating interactions across the network for retrieval. The percent connectivity was also calculated as the number of connections a node has in a given condition out of the total possible connections.

The authors found that functional connectivity, derived by measuring phase-synchronized low-frequency oscillations, was augmented both globally and in the parahippocampal gyrus (PHG) with successful retrieval of spatiotemporal memory. PPC of delta-theta frequency (1-10 Hz) range was greater for correct responses than incorrect. While percent connectivity increased throughout the network with successful retrieval, a disproportionately greater increase in the PHG node was also observed. PHG was designated a hub in the retrieval network. According to these findings, both network-wide and regional, but not frequency-specific, increases in functional connectivity occur for retrieval of spatiotemporal information. Comparing spatial versus temporal memory retrieval uncovered spectral, temporal, and regional segregation of functional connectivity within the retrieval network. For retrieval of spatial information, PPC and percent connectivity were increased between PHG, superior frontal gyrus (SFG), and middle frontal gyrus (MFG), and precuneus areas, at 1-4 Hz, and early in memory retrieval. Temporal memory retrieval was characterized by greater PPC and percent connectivity between PHG, SFG, MFG, and the inferior parietal lobule, at 7-10 Hz, and later in memory retrieval. The PHG was a hub in both conditions, making the same number of overall connections with other nodes, and with differential clustering of connectivity (Figure 1).

This work has notable implications for neuroscience and neurosurgery. The role of mesial temporal lobe structures (particularly the hippocampus) in memory recall remains controversial, particularly after memory consolidation. The hippocampus’s role in memory encoding is well established. Theories of consolidation typically argue that retrieval of consolidated information is independent of the hippocampus, while the Multiple Trace Theory (MTT) proposes that memory recall is hippocampus-dependent. The identification of the PHG, which is intimately connected with the hippocampus, as a hub, lends indirect support for MTT. Since the PHG includes connections from entorhinal, parahippocampal, and perirhinal cortices, but not the hippocampus proper, the evidence does not directly indicate specific action of the hippocampus but rather the MTL in general. Additionally, processes supporting functional connectivity and recall of distinct types of information were elucidated by the authors. This discovery could lead to clinical interventions targeting specific types of cognitive processes including memory retrieval. As neurosurgery continues to expand toward treating cognitive disorders, a network-level understanding of mechanisms and components of memory systems will prove invaluable.

Copyright © by the Congress of Neurological Surgeons