For whom the bell tolls: periodic reactivation of sensory cortex in the gamma band as a substrate of visual working memory maintenance

Abstract

Working memory (WM) is central to human cognition as it allows information to be kept online over brief periods of time and facilitates its usage in cognitive operations (Luck and Vogel, 2013). How this information maintenance actually is implemented is still a matter of debate. Several independent theories of WM, derived, respectively, from behavioral studies and neural considerations, advance the idea that items in WM decay over time and must be periodically reactivated. In this proposal, we show how recent data from intracranial EEG and attention research naturally leads to a simple model of such reactivation in the case of sensory memories. Specifically, in our model the amplitude of high-frequency activity (>50 Hz, in the gamma-band) underlies the representation of items in high-level visual areas. This activity decreases to noise-levels within 500 ms, unless it is reactivated. We propose that top-down attention, which targets multiple sensory items in a cyclical or rhythmic fashion at around 6–10 Hz, reactivates these decaying gamma-band representations. Therefore, working memory capacity is essentially the number of representations that can simultaneously be kept active by a rhythmically sampling attentional spotlight given the known decay rate. Since attention samples at 6–10 Hz, the predicted WM capacity is 3–5 items, in agreement with empirical findings.

EEG Cross-Frequency Phase Synchronization as an Index of Memory Matching in Visual Search

“…This adds to previous theoretical accounts that have strongly argued for a transient synchronization between theta and gamma phase over posterior electrode sites as a neuronal correlate of matching of incoming sensory information with memory contents from working memory (Sauseng et al, 2010(Sauseng et al, , 2015. It also lends evidence to the idea of sequential attentional templates (Lisman & Idiart, 1995;Olivers et al, 2011;Van Vugt et al, 2014). For future studies, it would be interesting to investigate the temporal dynamics of such matching processes during the acquisition and consolidation phase of attentional templates.…”

“…Assuming that we sequentially keep in mind multiple templates (Lisman & Idiart, 1995;Olivers et al, 2011;Van Vugt et al, 2014), memory matching should occur relatively early, a bit later or even much later in a given trial, depending on whether the sequence's first, second, or a later mental template could be matched to the current visual input. This means that in conditions where multiple mental templates could be matched to one out of several possible targets appearing on screen, the memory matching mechanism and likewise its resulting neuronal correlate, is supposed to display more temporal variability across trials.…”

Does cross‐frequency phase coupling of oscillatory brain activity contribute to a better understanding of visual working memory?

“…According to Van Vugt et al . (), this re‐activation of an item sequence after only a few theta cycles could be the mechanism by which WM capacity is limited. However, how could the findings reported by Vosskuhl et al .…”

“…However, in contrast to the aforementioned model (Jensen & Lisman, ; Lisman & Idiart, ), it is not assumed that separate memory items are represented by single gamma waves. Instead, it is suggested that each item is coded by an entire gamma burst, that is, multiple cycles, nested into a theta wave (Herman et al ., ; Van Vugt, Chakravarthi, & Lachaux, ). Consequently, only one item is coded per theta period, with multiple items retained sequentially in different subsequent theta cycles.…”

Current directions in visual working memory research: An introduction and emerging insights

“…Accordingly, the coupling of gamma and theta phase has been explored as a neuronal marker of VWM maintenance (Sauseng, Klimesch, et al ., ), and this idea was used to explain capacity limits and the (purported) slot‐like fashion of VWM storage: VWM capacity is limited by the number of complete gamma waves that can be nested within a theta cycle of a given length. Alternatively, according to a more recent proposal, items are coded as gamma bursts (i.e., multiple cycles; Herman, Lundqvist, & Lansner, ; Van Vugt, Chakravarthi, & Lachaux, ) and only one item is coded per theta period, with different items being refreshed in consecutive theta cycles. During a theta cycle, gamma amplitude first increases and then decreases, yielding a coupling of gamma amplitude to theta phase.…”