Riding the alpha wave - how auditory perception is shaped by oscillatory activity

Abstract

It is known since early psychophysiological research and an intriguing matter of fact that identical stimuli can elicit different neuronal responses and lead to varying percepts. The brain’s current state, which is reflected in the pattern of ongoing neuronal oscillations, thereby plays a key role. Growing evidence in the visual/somatosensory modality shows that particularly the alpha rhythm (an oscillation at about 10 Hz) defines the excitability of a certain brain region and systematically impacts on perception. While the decrease of alpha power points to increased excitability that facilitates perception the increase of alpha power has been related to the inhibition of the accordant brain region resulting in an inhibition or gating of perception. For the auditory modality, however, no such association has been established yet. Three studies were designed to investigate whether also auditory perception is dependent on the modulation of auditory alpha oscillations.The first study was carried out to examine the top-down modulation of the auditory cortex mediated by voluntary attention. Participants were visually cued to attend to either the left or right ear and after a short anticipation phase they had to distinguish target from standard tones at the respective ear. In line with the notion that an increase in alpha power reflects the gating of sensory information a prominent increase of low auditory alpha power in the hemisphere predominantly processing the to-be-ignored sound was found. The alpha power enhancement was further related to an increased synchronization between the strongly modulated auditory cortex and the right frontal eye fields described as key structure of the spatial attention network. Importantly, the condition-specific alpha power modulation in the auditory cortex was already present during anticipation of the auditory stimuli and thus mediated by mere top-down processes.These results led to another research question that is whether auditory perception is influenced automatically by bottom-up modulation of auditory alpha power. To address this within the second study the continuous perception of a phantom sound in tinnitus patients was altered by stimulation of the auditory cortex with Transcranial Magnetic Stimulation. The question was whether the perceptual changes are reflected in the modulation of auditory alpha activity. Strong decreases in tinnitus loudness were indeed related to increases in auditory alpha power at the stimulated site. This is in accordance with the notion that an increase of auditory alpha power is a crucial mechanism for gating auditory perception. The finding is further in line with the results of the first study that related increased auditory alpha power to a gating of external auditory stimuli.The third study was designed to examine whether and how oscillatory alpha activity is modulated when an auditory illusion is generated in healthy students. Therefore, auditory oscillatory activity to invariant sounds embedded in familiar as well as unfamiliar music was compared. Based on the fact that perception of continuity is facilitated by experience, it was hypothesized that noise within familiar music would be more likely to elicit a continuous percept of music than noise within unfamiliar music. Results indicated that this was indeed the case and that during the illusory perception of music alpha activity was reduced in the auditory cortex. This finding points to an increase of auditory cortex excitability favouring the experience of an illusory percept. Importantly, in this study it was shown that a decrease of auditory alpha power facilitated auditory perception emphasizing that auditory alpha power can indeed be modulated in both directions to either facilitate or gate perception. In addition to the auditory alpha power modulations, the auditory cortex increased its communication with the parahippocampal formation that likely stores the memory contents associated with the music illusion. It seems thus likely that neuronal activity in the highly excitable auditory cortex was shaped through the auditory-parahippocampal communication so that the illusion of continuing music was generated.Based on the three studies it can be concluded that auditory perception indeed depends on oscillatory alpha activity in the auditory cortex. Furthermore, the modulation of auditory alpha activity is related to the communication between the auditory cortex and non-auditory brain regions that are specific for different percepts or tasks (such as the spatial attention network or memory network). These findings are consistent with and extend findings concerning the impact of specific oscillatory activity patterns on perception from other modalities like the visual or somatosensory to the auditory. Last but not least, determining the signatures in auditory and non-auditory brain regions that are associated with improved auditory perception or pathological conditions such as tinnitus will serve as a basis for the development of effective interventions.