Abstract
Theta oscillations in the local field potential of neural ensembles are considered key mediators of human working memory. Theoretical accounts arising from animal hippocampal recordings propose that the phase of theta oscillations serves to instantiate sequential neuronal firing to form discrete representations of items held online. Human evidence of phase relationships in visual working memory has enhanced this theory, implicating long theta cycles in supporting greater memory capacity. Here we use human magnetoencephalographic recordings to examine a novel, alternative principle of theta functionality. The principle we hypothesize is derived from information theory and predicts that rather than long (low frequency) theta cycles, short (high frequency) theta cycles are best suited to support high information capacity. From oscillatory activity recorded during the maintenance period of a visual working memory task we show that a network of brain regions displays an increase in peak 4–12 Hz frequency with increasing memory load. Source localization techniques reveal that this network comprises bilateral prefrontal and right parietal cortices. Further, the peak of oscillation along this theta–alpha frequency axis is significantly higher in high capacity individuals compared to low capacity individuals. Importantly while we observe the adherence of cortical neuronal oscillations to our novel principle of theta functioning, we also observe the traditional inverse effect of low frequency theta maintaining high loads, where critically this was located in medial temporal regions suggesting parallel, dissociable hippocampal-centric, and prefrontal-centric theta mechanisms.
Highlights
Working memory (WM) is considered an essential cognitive resource, enabling the encoding, maintenance, and manipulation of information during short periods of time, facilitating action of current goals
From oscillatory activity recorded during the maintenance period of a visual working memory task we show that a network of brain regions displays an increase in peak 4–12 Hz frequency with increasing memory load
Previous event-related potentials (ERPs) (Vogel and Machizawa, 2004; Vogel et al, 2005) and Functional magnetic resonance imaging (fMRI) (Callicott et al, 1999; Todd and Marois, 2004) studies of visual WM (VWM) capacity indicate that neuronal measures correlating with item retention asymptote once capacity is attained, i.e., no further increase in activity is observed with increase in load
Summary
Working memory (WM) is considered an essential cognitive resource, enabling the encoding, maintenance, and manipulation of information during short periods of time, facilitating action of current goals. Neuroimaging studies of VWM have elaborated the neuroanatomical correlates of this capacity bottleneck. Functional magnetic resonance imaging (fMRI) studies demonstrate activity during VWM maintenance that saturates once capacity is reached in posterior parietal (Linden et al, 2003; Todd and Marois, 2004) and prefrontal cortices (Barch et al, 1997; Callicott et al, 1999), while inter-individual differences in memory capacity have been shown to correlate with signal changes in frontal regions and the basal ganglia (McNab and Klingberg, 2008). Electrophysiological studies of evoked brain responses demonstrate modulation by memory load that covaries with inter-individual differences in capacity, over posterior parietal and occipital sites (Vogel and Machizawa, 2004; Vogel et al, 2005; Ikkai et al, 2010)
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