Shaping functional architecture by oscillatory alpha activity: gating by inhibition

Abstract

In order to understand the working brain as a network, it is essential to identify the mechanisms by which information is gated between regions. We here propose that information is gated by inhibiting task-irrelevant regions, thus routing information to task-relevant regions. The functional inhibition is reflected in oscillatory activity in the alpha band (8-13 Hz). From a physiological perspective the alpha activity provides pulsed inhibition reducing the processing capabilities of a given area. Active processing in the engaged areas is reflected by neuronal synchronization in the gamma band (30-100 Hz) accompanied by an alpha band decrease. According to this framework the brain could be studied as a network by investigating cross-frequency interactions between gamma and alpha activity. Specifically the framework predicts that optimal task performance will correlate with alpha activity in task-irrelevant areas. In this review we will discuss the empirical support for this framework. Given that alpha activity is by far the strongest signal recorded by EEG and MEG, we propose that a major part of the electrophysiological activity detected from the working brain reflects gating by inhibition.

Keywords: alpha; effective connectivity; electroencephalography; functional connectivity; gamma; magnetoencephalography.

Figure 1

Different principles by which information can be gated through a network. Consider a situation in which information is supposed to be routed from node a to node b but not from node a to node c. (A) One possibility is that the synaptic connections from node a to b are strengthened on a fast time scale and weakened from node a to c. This would require a mechanism for synaptic plasticity that works on a fast time scale. (B) Information might be gated through neuronal phase-synchronization between node a and c. The information flow from node b to c is blocked by adjusting the phase difference. (C) We here promote the principle of gating by inhibition. Node c is actively suppressed by functional inhibition. This serves to gate the information flow from a to b. The functional inhibition is reflected in the 9–13 Hz alpha band.

Figure 2

Posterior alpha activity increases when the ventral stream, but not the dorsal stream, is engaged. (A) In a delayed-match-to-sample task subjects were asked to either maintained the identity (ID) or orientation (OR) of a presented face. (B) Time–frequency representations of power of the MEG signal over posterior regions measured during the task. Alpha activity increased in the ID task engaging the ventral stream, but remained low in the OR task engaging the dorsal stream. (C) The topographies of the alpha power showed that the increase in the ID condition was stronger over posterior central regions. (D) A beamforming analysis identified the alpha increase to parieto-occipital areas. The findings support the notion that the dorsal stream is suppressed by alpha activity when the ventral stream is engaged. Figure adapted from Jokisch and Jensen (2007).

Figure 3

Alpha activity in non-engaged sensorimotor areas predicts performance in a somatosensory working memory task. (A) Sample patterns of electrical stimuli were presented to the right hand. After a 2-s retention period subjects had to answer whether the frequency of the probe stimulus was higher or lower. (B) The 8–13 Hz alpha activity in the retention interval was compared with respect to correct and incorrect responses. The right hemisphere alpha activity was stronger for successful performance. (C) Time–frequency representations of power showed that the task-dependent effect was constrained to the alpha band in the retention interval. (D) The sources of the task-dependent alpha activity were localized in right sensorimotor and parieto-occipital regions. Reproduced from Haegens et al. (2009).

Figure 4

We hypothesize that alpha activity serves to functionally disengage a given region by means of “pulsed inhibition.” Consider the ongoing gamma rhythm in the lower trace which reflects neuronal processing. The pulsed alpha inhibition temporarily silences the gamma activity. As alpha goes stronger, the “duty-cycle” of gamma and thus neuronal computation decreases gradually. Reproduced from Osipova et al. (2008).