Oscillatory infrasonic modulation of the cochlear amplifier by selective attention.

Constantino D Dragicevic,Paul H Delano,Bruno Marcenaro,Luis Robles,Marcela Navarrete,Manuel S Malmierca

doi:10.1371/journal.pone.0208939

Abstract

Evidence shows that selective attention to visual stimuli modulates the gain of cochlear responses, probably through auditory-cortex descending pathways. At the cerebral cortex level, amplitude and phase changes of neural oscillations have been proposed as a correlate of selective attention. However, whether sensory receptors are also influenced by the oscillatory network during attention tasks remains unknown. Here, we searched for oscillatory attention-related activity at the cochlear receptor level in humans. We used an alternating visual/auditory selective attention task and measured electroencephalographic activity simultaneously to distortion product otoacoustic emissions (a measure of cochlear receptor-cell activity). In order to search for cochlear oscillatory activity, the otoacoustic emission signal, was included as an additional channel in the electroencephalogram analyses. This method allowed us to evaluate dynamic changes in cochlear oscillations within the same range of frequencies (1–35 Hz) in which cognitive effects are commonly observed in electroencephalogram works. We found the presence of low frequency (<10 Hz) brain and cochlear amplifier oscillations during selective attention to visual and auditory stimuli. Notably, switching between auditory and visual attention modulates the amplitude and the temporal order of brain and inner ear oscillations. These results extend the role of the oscillatory activity network during cognition in neural systems to the receptor level.

Highlights

In natural environments animals are surrounded by a variety of sensory stimuli
During the period of auditory selective attention, in which subjects had high expectancy for a silence gap embedded in the continuous distortion product otoacoustic emissions (DPOAE)-evoking primary tones (f1 and f2), an evoked potential appeared in the grand average of the EEG signal at Cz (Fig 2A), while in the same period a subtle non-significant reduction was observed in the DPOAE signal (Fig 2B)
We found the presence of low frequency oscillations (

Summary

Introduction

In natural environments animals are surrounded by a variety of sensory stimuli. As the nervous system has a limited capacity for processing all sensory stimuli, individuals require of attention to focus their cognitive resources on the most relevant. The gain control of sensory responses by attention is probably the principal mechanism of attentional selection, this process does not explain all of the neural modulations observed during attention, since the nervous system could use additional mechanisms for the selection of a relevant stimulus [5,6,7,8]. Whether cortical oscillations modulate cochlear responses at the receptor level during selective attention to visual stimuli is unknown. We used an alternating visual/auditory selective attention task in humans (based on [17]) and measured electroencephalographic (EEG) activity simultaneously to a virtual channel of the amplitude of distortion product otoacoustic emissions (DPOAE) that allowed us to examine in the frequency domain, the single-trial dynamics between cortical electrical oscillations and hypothetical oscillatory activity of the cochlear amplifier [18,19]

Results

Discussion

Participants