Alpha power indexes task-related networks on large and small scales: A multimodal ECoG study in humans and a non-human primate

Abstract

Performing different tasks, such as generating motor movements or processing sensory input, requires the recruitment of specific networks of neuronal populations. Previous studies suggested that power variations in the alpha band (8–12 Hz) may implement such recruitment of task-specific populations by increasing cortical excitability in task-related areas while inhibiting population-level cortical activity in task-unrelated areas (Klimesch et al., 2007; Jensen and Mazaheri, 2010). However, the precise temporal and spatial relationships between the modulatory function implemented by alpha oscillations and population-level cortical activity remained undefined. Furthermore, while several studies suggested that alpha power indexes task-related populations across large and spatially separated cortical areas, it was largely unclear whether alpha power also differentially indexes smaller networks of task-related neuronal populations. Here we addressed these questions by investigating the temporal and spatial relationships of electrocorticographic (ECoG) power modulations in the alpha band and in the broadband gamma range (70–170 Hz, indexing population-level activity) during auditory and motor tasks in five human subjects and one macaque monkey. In line with previous research, our results confirm that broadband gamma power accurately tracks task-related behavior and that alpha power decreases in task-related areas. More importantly, they demonstrate that alpha power suppression lags population-level activity in auditory areas during the auditory task, but precedes it in motor areas during the motor task. This suppression of alpha power in task-related areas was accompanied by an increase in areas not related to the task. In addition, we show for the first time that these differential modulations of alpha power could be observed not only across widely distributed systems (e.g., motor vs. auditory system), but also within the auditory system. Specifically, alpha power was suppressed in the locations within the auditory system that most robustly responded to particular sound stimuli. Altogether, our results provide experimental evidence for a mechanism that preferentially recruits task-related neuronal populations by increasing cortical excitability in task-related cortical areas and decreasing cortical excitability in task-unrelated areas. This mechanism is implemented by variations in alpha power and is common to humans and the non-human primate under study. These results contribute to an increasingly refined understanding of the mechanisms underlying the selection of the specific neuronal populations required for task execution.

Functional localization and effective connectivity of cortical theta and alpha oscillatory activity during an attention task

“…This interpretation is in line with the inhibitory role of alpha oscillations (De Pesters et al, 2016, Klimesch et al, 2007, Pfurtscheller and Da Silva, 1999). …”

“…This property can be expressed, for instance, in the form of an inhibition of distant task-irrelevant regions by means of an increase of alpha activity (De Pesters et al, 2016). …”

Spatial specificity of alpha oscillations in the human visual system

“…This is in line with recent findings from human and animal intracranial recordings demonstrating the spatial specificity of alpha activity in the auditory domain. Task‐relevant alpha power is differentially modulated within the auditory system in accordance with differential sound input and relates to population‐level activity (de Pesters et al, ). Thus, the spatial tuning reported here potentially reflects the allocation of spatial attention by setting the gain in a regionally specific sense such that processing of upcoming targets are facilitated while distractors are inhibited.…”

Instantaneous voltage as an alternative to power- and phase-based interpretation of oscillatory brain activity

“…These studies suggest that the power or phase of oscillatory activity modulates the level of cortical activity or behavioral performance [6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32] and hence plays a central role in the dynamic modulation of cortical function in response to varying task demands [33, 34, 35]. Specifically, these and other studies have consistently reported that during times when oscillatory power is low or during times of an oscillatory trough, the probability of action potential firing rate, broadband gamma augmentation, or higher behavioral performance is increased 2 .…”