Oscillation Phase Locking and Late ERP Components of Intracranial Hippocampal Recordings Correlate to Patient Performance in a Working Memory Task.

Jonathan K Kleen,Gregory L Holmes,Markus E Testorf,David W Roberts,Pierre-Pascal Lenck-Santini,Barbara J Jobst,Rod C Scott

doi:10.3389/fnhum.2016.00287

Abstract

In working memory tasks, stimulus presentation induces a resetting of intracranial temporal lobe oscillations in multiple frequency bands. To further understand the functional relevance of this phenomenon, we investigated whether working memory performance depends on the phase precision of ongoing oscillations in the hippocampus. We recorded intra-hippocampal local field potentials in individuals performing a working memory task. Two types of trials were administered. For high memory trials presentation of a list of four letters (“List”) was followed by a single letter memory probe (“Test”). Low memory load trials, consisting of four identical letters (AAAA) followed by a probe with the same letter (A), were interspersed. Significant phase locking of ongoing oscillations across trials, estimated by the Pairwise Phase Consistency Index (PPCI) was observed in delta (0.5–4 Hz), theta (5–7 Hz), and alpha (8–12 Hz) bands during stimulus presentation and recall but was increased in low memory load trials. Across patients however, higher delta PPCIs during recall in the left hippocampus were associated with faster reaction times. Because phase locking could also be interpreted as a consequence of a stimulus evoked potential, we performed event related potential analysis (ERP) and examined the relationship of ERP components with performance. We found that both amplitude and latency of late ERP components correlated with both reaction time and accuracy. We propose that, in the Sternberg task, phase locking of oscillations, or alternatively its ERP correlate, synchronizes networks within the hippocampus and connected structures that are involved in working memory.

Highlights

There is increasing evidence that oscillatory activity in the hippocampus plays a major role in learning and memory
We report that phase locking in delta, theta, and alpha frequency bands increases after task stimulus presentation, but that phase consistency does not decrease in trials with lower memory load
We investigated whether hippocampal phase reset of oscillations after stimulus presentation in a working memory task was correlated with performance

Summary

Introduction

There is increasing evidence that oscillatory activity in the hippocampus plays a major role in learning and memory. In the Sternberg working memory task theta power is increased in temporal lobe intracranial electrodes during stimulus presentation, as opposed to inter-trial intervals (Raghavachari et al, 2001). In this task, participants are presented with a list of items to memorize and asked, after a delay, to determine whether test items were present in the list. It has been demonstrated that the presentation of stimuli that are to be encoded and those that constitute a retrieval cue generate a resetting of theta oscillations at different phases (Rizzuto et al, 2006). Together with studies performed in rodents (Adey and Walter, 1963; Givens, 1996; Vinogradova et al, 1996; Holscher et al, 1997; Hyman et al, 2003; McCartney et al, 2004), these results support the notion that phase reset of ongoing theta oscillations ensures that information is transmitted at a phase that is optimal for memory processing

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