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

Abstract

Extensive work in humans using magneto-and electroencephalography strongly suggests that decreased oscillatory α-activity (8-14 Hz) facilitates processing in a given region, whereas increased α-activity serves to actively suppress irrelevant or interfering processing. However, little work has been done to understand how α-activity is linked to neuronal firing. Here, we simultaneously recorded local field potentials and spikes from somatosensory, premotor, and motor regions while a trained monkey performed a vibrotactile discrimination task. In the local field potentials we observed strong activity in the α-band, which decreased in the sensorimotor regions during the discrimination task. This α-power decrease predicted better discrimination performance. Furthermore, the α-oscillations demonstrated a rhythmic relation with the spiking, such that firing was highest at the trough of the α-cycle. Firing rates increased with a decrease in α-power. These findings suggest that α-oscillations exercise a strong inhibitory influence on both spike timing and firing rate. Thus, the pulsed inhibition by α-oscillations plays an important functional role in the extended sensorimotor system.T he prominent posterior α-rhythm (8-14 Hz) was first described by Hans Berger (1) and long considered to reflect cortical idling (2, 3). To a large extent, the α-rhythm has been ignored by animal neurophysiologists (but see ref. 4) and considered to be of little functional relevance. Thus, it remains largely unknown how ongoing α-oscillations relate to neuronal firing.In contrast to the idling hypothesis, converging electrophysiological evidence in humans suggests that α-oscillations play an important functional role in cognitive processing (5-7). In particular, α-activity might serve to shape the state of sensory brain regions to direct the flow of information and optimize performance (8). In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9-14) and influences detection performance (15-17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18-21). Furthermore, α-activity has been implicated in visual (22-25), auditory (26), and somatosensory working-memory performance (27).These studies strongly suggest that decreased α-activity facilitates processing in task-relevant brain regions, whereas increased α-activity functions to suppress distracting input in task-irrelevant regions. However, given the strong oscillatory nature of the α-activity, it is less clear how it influences processing in a phasic manner. It has been suggested that α-oscillations serve to depress processing every ∼100 ms by a mechanism of pulsed inhibition (5,(28)(29)(30). In support of this notion, it has recently been demonstrated that perception is modulated by the prestimulus phase of the α-rhythm (31, 32). Likewise, it was recently shown that the magnitude of the blood-oxygen level-dependent signal in response to a visual...

Alpha-Band Brain Oscillations Shape the Processing of Perceptible as well as Imperceptible Somatosensory Stimuli during Selective Attention

“…With respect to the attention effect on pre-mu activity, our results are in line with several studies reporting that attention leads to a decrease of alpha power contralateral to where spatial attention is directed compared with ipsilateral sites (somatosensory: Pfurtscheller and Lopes da Silva, 1999;Jones et al, 2010;Anderson and Ding, 2011;Haegens et al, 2011aHaegens et al, , 2012visually: Thut et al, 2006;auditory: Weisz et al, 2014;Wöstmann et al, 2016). This strongly supports the assumption of selective attention relying on intrinsic oscillatory activity in the somatosensory cortex already before the incoming stimulus (Thut et al, 2006).…”

“…Both linear (Nikouline et al, 2000b;Reinacher et al, 2009;Roberts et al, 2014) and nonlinear relationships (Zhang and Ding, 2010;Anderson and Ding, 2011) have been reported. Although the latter findings challenge the view of alpha activity directly reflecting cortical excitation (Jensen and Mazaheri, 2010;Foxe and Snyder, 2011), one might still argue that the variation of prestimulus alpha activity in spatial attention leads to a modulation of evoked activity (Jones et al, 2010; Haegens et al, 2011aHaegens et al, , 2012. Consequently, with attention, the highest P1 amplitudes should be accompanied by low prestimulus alpha power in the case of a linear relationship, or alternatively, by intermediate power ranges in the nonlinear case (Anderson and Ding, 2011).…”

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

“…Moreover, we found that trials with more LFP α-power (5-15 Hz) had a weaker MUA response ( Fig. 2E) (corrected coefficient = −0.05, t test, n = 493, P < 0.05) (36) in further support of this idea.…”

Beyond establishing involvement: quantifying the contribution of anticipatory α- and β-band suppression to perceptual improvement with attention

“…These properties suggest that oscillatory amplitude modulation reflects an important mechanism underlying the orienting of attention. This is further supported by the observation that low amplitude in the ␣-and ␤-band is associated with an enhancement in 1) cortical excitability (Haegens et al 2011b;Romei et al 2008;Sauseng et al 2009), 2) blood oxygenation level-dependent (BOLD) activity (Ritter et al 2009;Scheeringa et al 2011), and 3) psychophysical performance in visual (Thut et al 2006;van Dijk et al 2008) and tactile (Haegens et al 2011a;Jones et al 2010;van Ede et al 2011) tasks.…”