Top-Down Controlled Alpha Band Activity in Somatosensory Areas Determines Behavioral Performance in a Discrimination Task

Abstract

The brain receives a rich flow of information which must be processed according to behavioral relevance. How is the state of the sensory system adjusted to up-or downregulate processing according to anticipation? We used magnetoencephalography to investigate whether prestimulus alpha band activity (8 -14 Hz) reflects allocation of attentional resources in the human somatosensory system. Subjects performed a tactile discrimination task where a visual cue directed attention to their right or left hand. The strength of attentional modulation was controlled by varying the reliability of the cue in three experimental blocks (100%, 75%, or 50% valid cueing). While somatosensory prestimulus alpha power lateralized strongly with a fully predictive cue (100%), lateralization was decreased with lower cue reliability (75%) and virtually absent if the cue had no predictive value at all (50%). Importantly, alpha lateralization influenced the subjects' behavioral performance positively: both accuracy and speed of response improved with the degree of alpha lateralization. This study demonstrates that prestimulus alpha lateralization in the somatosensory system behaves similarly to posterior alpha activity observed in visual attention tasks. Our findings extend the notion that alpha band activity is involved in shaping the functional architecture of the working brain by determining both the engagement and disengagement of specific regions: the degree of anticipation modulates the alpha activity in sensory regions in a graded manner. Thus, the alpha activity is under top-down control and seems to play an important role for setting the state of sensory regions to optimize processing.

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

“…We found that decreases in α-activity during the decision period correlated with task performance in S1, S2, DPC, MPC-left, and M1. The current findings are consistent with previous work showing that somatosensory α-activity influences discrimination performance (18,27) and with the visuospatial attention literature linking α-activity to detection performance (15)(16)(17). These previous findings have resulted in the notion that α-activity is involved in sensory gating.…”

“…In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9)(10)(11)(12)(13)(14) and influences detection performance (15)(16)(17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18)(19)(20)(21). Furthermore, α-activity has been implicated in visual (22)(23)(24)(25), auditory (26), and somatosensory working-memory performance (27).…”

Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions

“…We found a similar negative relationship between alpha and reporting of touch over ipsilateral somatosensory cortex on touch absent trials as we found over contralateral cortex. Alpha over sensory regions other than the primary region associated with a task may play a key role in suppressing irrelevant information -the gating-by-inhibition hypothesis -as seen in a number of studies of spatial attention (Gray, Frey, Wilson, & Foxe, 2015;Haegens et al, 2011Haegens et al, , 2011Jensen & Mazaheri, 2010). Thus, when attending to the right hand, alpha power increases over right, ipsilateral somatosensory cortices and decreases over left, contralateral somatosensory cortices.…”

“…Alpha oscillations may thus reflect pulses of cortical inhibition (Mathewson et al, 2011), as a sensory region adjusts to temporal expectations of the delivery of a stimulus by ensuring it is in high-excitability state when a stimulus is expected. Top-down manipulation of alpha power may also be a mechanism for the suppression of irrelevant stimuli (Haegens, Händel, & Jensen, 2011), through the inhibition of cortical regions dealing with, for example, unattended regions of space. This may also be used to gate communication between different cortical regions (Jensen, Bonnefond, & VanRullen, 2012;Jensen & Mazaheri, 2010), allowing or preventing early sensory responses to reach consciousness (Weisz et al, 2014).…”

Peripersonal space boundaries around the lower limbs

“…The reason for this manipulation was to control for the effects of expectancy during the task, which has been shown to modulate the activity of cortical sensorimotor areas [thereby affecting response times; e.g. Haegens et al (2011)]. Moreover, recent investigations in our lab have revealed that the optimal ratio of real to catch trials in this paradigm is 1:1 (Kandula et al 2017).…”