Functional Dissociation of Ongoing Oscillatory Brain States

Neda Salari,Christian Büchel,Michael Rose,Thomas Boraud

doi:10.1371/journal.pone.0038090

Neda Salari, Christian Büchel + Show 2 more

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https://doi.org/10.1371/journal.pone.0038090

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Abstract

The state of a neural assembly preceding an incoming stimulus is assumed to modulate the processing of subsequently presented stimuli. The nature of this state can differ with respect to the frequency of ongoing oscillatory activity. Oscillatory brain activity of specific frequency range such as alpha (8–12 Hz) and gamma (above 30 Hz) band oscillations are hypothesized to play a functional role in cognitive processing. Therefore, a selective modulation of this prestimulus activity could clarify the functional role of these prestimulus fluctuations. For this purpose, we adopted a novel non-invasive brain-computer-interface (BCI) strategy to selectively increase alpha or gamma band activity in the occipital cortex combined with an adaptive presentation of visual stimuli within specific brain states. During training, oscillatory brain activity was estimated online and fed back to the participants to enable a deliberate modulation of alpha or gamma band oscillations. Results revealed that volunteers selectively increased alpha and gamma frequency oscillations with a high level of specificity regarding frequency range and localization. At testing, alpha or gamma band activity was classified online and at defined levels of activity, visual objects embedded in noise were presented instantly and had to be detected by the volunteer. In experiment I, the effect of two levels of prestimulus gamma band activity on visual processing was examined. During phases of increased gamma band activity significantly more visual objects were detected. In experiment II, the effect was compared against increased levels of alpha band activity. An improvement of visual processing was only observed for enhanced gamma band activity. Both experiments demonstrate the specific functional role of prestimulus gamma band oscillations for perceptual processing. We propose that the BCI method permits the selective modulation of oscillatory activity and the direct assessment of behavioral consequences to test for functional dissociations of different oscillatory brain states.

Highlights

The state of a neural ensemble directly preceding an incoming stimulus has a prominent impact on the quality of the processing of that stimulus
We focused on the role of gamma band oscillations over the lateral occipital cortex (LOC) for the subsequent processing of visual object stimuli
The present study examined the functional relevance of gamma band oscillations in the visual cortex for subsequent visual object processing

Summary

Introduction

The state of a neural ensemble directly preceding an incoming stimulus has a prominent impact on the quality of the processing of that stimulus. A relevant amount of the variability of human task performance can be attributed to intrinsic fluctuations of neural activity prior to actual task processing [1,2,3,4,5,6]. These intrinsic fluctuations can be characterized by the frequency range of ongoing electrophysiological activity as measured with EEG. Other studies indicate a functional relevance of alpha band oscillations for visual processing [13,14,15,16]

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