Transcranial Magnetic Stimulation Reveals Intrinsic Perceptual and Attentional Rhythms

Abstract

Oscillatory brain activity has functional relevance for perceptual and cognitive processes, as proven by numerous electrophysiology studies accumulating over the years. However, only within the past two decades have researchers been able to study the causal role of such oscillations using transcranial magnetic stimulation (TMS) technology. Two complementary approaches exist. A majority of research employs rhythmic TMS (rTMS) to entrain oscillatory activity and investigate its effect on targeted brain functions. On the other hand, single pulses of TMS (spTMS) that can be delivered with a high spatio-temporal resolution, can be used to precisely probe the state of the system. In this mini-review, we concentrate on this second approach. We argue that, with no a priori hypothesis on the oscillatory frequency of the targeted cortical regions, spTMS can help establish causal links between spontaneous oscillatory activity and perceptual and cognitive functions. Notably, this approach helped to demonstrate that the occipital cortex is periodically involved during specific attentional tasks at the theta (~5 Hz) frequency. We propose that this frequency reflects periodic inter-areal communication for attentional exploration and selection. In the future, clever combination of non-invasive recording and stimulation with well-controlled psychophysics protocols will allow us to further our understanding of the role of brain oscillations for human brain functions.

Attention explores space periodically at the theta frequency

“…sensory rhythm (~11 Hz; whose phase may not be reset by stimulus onset, or only partially), would coexist with the theta attentional rhythm (~4 Hz), and either be recordable concurrently or be masked depending on task relevance. This is consistent with recent literature reviews suggesting that theta corresponds to the rhythm of attentional exploration while alpha rather reflects an ongoing, sensory sampling rhythm (Davidson, Alais, Boxtel, & Tsuchiya, 2018;Dugué & VanRullen, 2017;VanRullen, 2016).…”

“…Similarly, we recently proposed that theta rhythmicity may emerge from iterative connections between sensory and attentional regions (Dugué et al, in print;Dugué & VanRullen, 2017).…”

“…Despite the impression that our visual perception is seamless and continuous across time, mounting evidence suggests that this is an illusion; information is sampled periodically at low frequencies (theta: 4-7 Hz and alpha: 8-12 Hz). Specifically, the alpha and theta rhythms seem to coexist in the brain and support different functions (Dugué, Beck, Marque, & VanRullen, in print;Dugué & VanRullen, 2017;Dugué, Xue, & Carrasco, 2017;VanRullen, 2016). Alpha has been related to sensory aspects of visual perception, and was first described as the natural frequency of the occipital pole (Rosanova et al, 2009).…”

“…Theta appears to be related to attentional sampling (for review VanRullen, 2016). Specifically, a series of recent research used exploration tasks including visual search (Dugué, Marque, & VanRullen, 2015;Dugué, McLelland, Lajous, & VanRullen, 2015;Dugué & VanRullen, 2014;Dugué, Xue, et al, 2017), priming (Huang, Chen, & Luo, 2015), exogenous (involuntary) spatial attention (Chen, Wang, Wang, Tang, & Zhang, 2017;Landau & Fries, 2012;Landau, Schreyer, van Pelt, & Fries, 2015), endogenous (voluntary) spatial (Song, Meng, Chen, Zhou, & Luo, 2014) and feature-based attention (Fiebelkorn, Pinsk, & Kastner, 2018;Fiebelkorn, Saalmann, & Kastner, 2013;Helfrich et al, 2018) tasks, designed to manipulate covert attention -selective processing of information in the absence of eye movements (Carrasco, 2011(Carrasco, , 2014 -and suggested that visual information is sampled periodically at the theta frequency when attentional exploration of the visual space is required (for review see Dugué & VanRullen, 2017).…”

Entrainment of local synchrony reveals a causal role for high-beta right frontal oscillations in human visual consciousness

“…Within the last decade, there has been increasing interest in the involvement of oscillations and synchronization in information coding (Buzsaki and Draguhn, 2004;Fries et al, 2007). In the research field of attention and perception, occipital or parietal alpha (Thut et al, 2006;Marshall et al, 2015) and theta (Dugue and VanRullen, 2017), fronto-parietal beta (Buschman and Miller, 2007;Phillips and Takeda, 2009), occipital and fronto-parietal gamma synchrony (Buschman and Miller, 2007;Wyart and Tallon-Baudry, 2009;Marshall et al, 2015) and fronto-parietal rhythmic states coordinated by theta oscillations (Fiebelkorn et al, 2018) have been associated with the ability to acknowledge the presence of a visual target.…”