Oscillatory correlates of auditory working memory examined with human electrocorticography

Abstract

This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschl's gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior-and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. The work demonstrates sustained activity patterns that can only be explained by AWM maintenance, with prominent lowfrequency increases in medial temporal lobe regions.

How Can Hearing Loss Cause Dementia?

“…However, these did not require an active task, which the visual literature suggests may be necessary; further work is needed. However, supporting a role of the hippocampus in pattern analysis, auditory working memory for tone frequency engages the hippocampus (Kumar et al, 2016(Kumar et al, , 2020 and correlates with speech-in-noise ability (Lad et al, 2020). Phonological working memory also correlates with speech-in-noise ability (Akeroyd, 2008), although there has been debate about this (F€ ullgrabe and Rosen, 2016).…”

“…The human hippocampus is also involved in working memory processes that are required for the analysis of acoustic patterns that evolve over time. Functional imaging (Kumar et al, 2016) has demonstrated increased blood-oxygen-level-dependent (BOLD) activity in the hippocampus when subjects hold tones in mind, and human local field potential recordings (Kumar et al, 2020) have demonstrated low-frequency oscillatory activity during the same process. Representations of auditory content are also available to the hippocampus during active listening.…”

The hearing hippocampus

“…Comparable findings linking unit activity to oscillatory phase or particular timepoints are yet to be reported for auditory memoranda, however the degree of synchrony among groups of neurons in rat CA1 can distinguish a tone frequency held in memory from another, even when such information is not carried in the firing rate of individual neurons (Takahashi and Sakurai, 2009). In humans, increases in hippocampal BOLD activity (Kumar et al, 2016) and low frequency oscillatory power (Kumar et al, 2021) emerge when human subjects keep a tone frequency in mind for comparison to a probe. It has been argued that the hippocampus is involved in retention over a few seconds only when the stimuli require complex highresolution binding (Yonelinas, 2013) or additional demands are placed on working memory (Jeneson and Squire, 2011), but neither were the case in the Kumar et al (2021) study.…”

“…In humans, increases in hippocampal BOLD activity (Kumar et al, 2016) and low frequency oscillatory power (Kumar et al, 2021) emerge when human subjects keep a tone frequency in mind for comparison to a probe. It has been argued that the hippocampus is involved in retention over a few seconds only when the stimuli require complex highresolution binding (Yonelinas, 2013) or additional demands are placed on working memory (Jeneson and Squire, 2011), but neither were the case in the Kumar et al (2021) study.…”

Neural dynamics underlying successful auditory short‐term memory performance

“…Recent years have shown an increasing interest in human ASTM (Arnott et al, 2005;Buchsbaum et al, 2005;Cappotto et al, 2021;Kumar et al, 2016;Lim et al, 2022;Noyce et al, 2022;Papagno et al, 2017), particularly in the context of electrophysiological oscillatory correlates (Kaiser, 2015;Kumar et al, 2021;Weisz et al, 2020;Wilsch & Obleser, 2016). Although previous work has predominantly focused on contrasting low-and high-load ASTM tasks, here, we ask what patterns of brain activity distinguish successful versus unsuccessful ASTM performance while the task, and stimuli presented to participants, remain fixed.…”