Oscillatory activity in parietal and dorsolateral prefrontal cortex during retention in visual short‐term memory: Additive effects of spatial attention and memory load

Abstract

We used whole-head magnetoencephalography to study the representation of objects in visual short-term memory (VSTM) in the human brain. Subjects remembered the location and color of either two or four colored disks that were encoded from the left or right visual field (equal number of distractors in the other visual hemifield). The data were analyzed using time-frequency methods, which enabled us to discover a strong oscillatory activity in the 8-15 Hz band during the retention interval. The study of the alpha power variation revealed two types of responses, in different brain regions. The first was a decrease in alpha power in parietal cortex, contralateral to the stimuli, with no load effect. The second was an increase of alpha power in parietal and lateral prefrontal cortex, as memory load increased, but without interaction with the hemifield of the encoded stimuli. The absence of interaction between side of encoded stimuli and memory load suggests that these effects reflect distinct underlying mechanisms. A novel method to localize the neural generators of load-related oscillatory activity was devised, using cortically-constrained distributed source-localization methods. Some activations were found in the inferior intraparietal sulcus (IPS) and intraoccipital sulcus (IOS). Importantly, strong oscillatory activity was also found in dorsolateral prefrontal cortex (DLPFC). Alpha oscillatory activity in DLPFC was synchronized with the activity in parietal regions, suggesting that VSTM functions in the human brain may be implemented via a network that includes bilateral DLPFC and bilateral IOS/IPS as key nodes.

Flexible frequency control of cortical oscillations enables computations required for working memory

“…We designed a bihemispheric spiking network to explain the lateralization of alpha frequency in delayed-response tasks where relevant and irrelevant information are segregated in different hemifields (8,16,17). These experimental results show that alpha activity increases in the hemispheres encoding irrelevant information.…”

“…On the other hand, suppression of irrelevant information is associated with oscillations in the alpha band (8)(9)(10)(11)(12)(13). In lateralized WM tasks where the subject should ignore cues in one hemifield, alpha power increases in the hemisphere encoding such irrelevant information (8,16,17). However, a mechanistic theory explaining why oscillations of various frequency bands wax and wane in time and space during effortful tasks and in particular WM remains outstanding.…”

“…Recently it has been speculated that individual bands may implement elementary computations constituent in cognitive tasks (1, 2) as is seen during working memory (WM) performance. Human electrophysiology studies show clearly that memory maintenance correlates positively with oscillations in the theta band (4)(5)(6)(7)(8), in the beta band (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) ref. 9), and in the gamma band .…”

Oscillatory activity in prefrontal and posterior regions during implicit letter-location binding

“…However, an alternative interpretation is possible since several authors propose that the prefrontal cortex does not maintain mnemonic representations (Lebedev et al, 2004;Owen et al, 1998;Petrides, 2000;Rissman et al, 2008;Rowe and Passingham, 2001). Instead, prefrontal cortex is considered to participate in controlled processing of the activity of posterior brain regions more directly involved in representing specific features as well as categorical information (Doesburg et al, 2009;Grimault et al, 2009;Kessler and Kiefer, 2005;Mechelli et al, 2004;Rainer and Ranganath, 2002;Serences and Yantis, 2006). This control could be exerted by means of longrange fronto-posterior connections (Grimault et al, 2009;Hasegawa et al, 2000;Kessler and Kiefer, 2005).…”

“…Although neural oscillatory activity in the gamma band was originally proposed as the mechanism underlying binding processes (Singer, 2001;Singer and Gray, 1995;Tallon-Baudry and Bertrand, 1999), oscillations in other "classical" frequency ranges (theta, alpha and beta) have also been linked with visual-feature binding and cross-modal binding (Bassett et al, 2006;Hummel and Gerloff 2005;Mima et al, 2001;Palva et al, 2005;Wu et al, 2007). While it has been shown that WM operations engage oscillations in different frequency ranges (Grimault et al, 2009;Jokisch and Jensen, 2007;Sauseng et al, 2004;Tesche and Karhu, 2000), the actual role of each frequency in representing the contents of WM remains unclear (Kahana, 2006;Palva et al, 2005). As the neural dynamics required for cross-code integrated representations presumably demands interactions between activities of multiple brain regions in different frequency ranges (Calvert et al, 2000;Doesburg et al, 2008a;Palva et al, 2005), here, we propose that neuronal oscillatory activity in various frequencies should be greater when verbal and spatial features are maintained as an integrated representation.…”