Elsevier

NeuroImage

Volume 60, Issue 1, March 2012, Pages 170-178
NeuroImage

It's only in your head: Expectancy of aversive auditory stimulation modulates stimulus-induced auditory cortical alpha desynchronization

https://doi.org/10.1016/j.neuroimage.2011.12.034Get rights and content

Abstract

Increasing evidence underlines the functional importance of non-phase-locked cortical oscillatory rhythms. Among the different oscillations, alpha (8–12 Hz) has been shown to be modulated by anticipation or attention, suggesting a top-down influence. However, most studies to date have been conducted in the visual modality and the extent to which this notion also applies to the auditory cortex is unclear. It is furthermore often difficult to dissociate bottom-up from top-down contributions in cases of different stimuli (e.g., standards vs. deviants) or stimuli that are preceded by different cues. This study addresses these issues by investigating neuronal responses associated with intrinsically fluctuating perceptions of an invariant sound. Sixteen participants performed a pseudo-frequency-discrimination task in which a “high-pitch” tone was followed by an aversive noise, while the “low-pitch” tone was followed by silence. The participants had to decide which tone was presented even though the stimulus was actually kept constant while pseudo-randomized feedback was given. EEG data show that auditory cortical alpha power decreased by 20% in “high-pitch” trials relative to trials in which a “low pitch” was perceived. This study shows that expectancy of aversive feedback modulates perception of sounds and these fluctuating perceptions become manifest in modulations of sound-related alpha desynchronizations. Our findings extend recent evidence in the visual and somatosensory domain that alpha oscillations represent the excitatory/inhibitory balance of sensory cortical cell assemblies, which can be tuned in a top-down manner.

Introduction

An increasing amount of empirical evidence underlines the functional importance of oscillatory rhythms that are not phase-locked to an external stimulus (Bollimunta et al., 2008, Buzsáki and Draguhn, 2004, Min and Herrmann, 2007, Thut et al., 2006). It has been shown that these induced rhythms have a significant impact on the processing of the stimulus and have the potential to explain – at least in parts – the behavioral trial-by-trial variability (Linkenkaer-Hansen et al., 2004, Romei et al., 2008b, Sauseng et al., 2009). In this study, we show that expectancy shapes perception as well as auditory cortical alpha oscillations (8–12 Hz) during the processing of an invariant sound.

Experiments in cognitive neuroscience usually compare neuronal responses to well-defined experimental conditions while discarding trial-to-trial fluctuations as noise. However, an increasing amount of evidence underlines the functional relevance of fluctuating oscillatory brain activity, for instance in the motor, somatosensory and visual cortices. This relationship has been researched in the pre-stimulus period (e.g., Linkenkaer-Hansen et al., 2004, Romei et al., 2008a, Sauseng et al., 2009) as well as in the post-stimulus period (e.g., Gross et al., 2007). In the presented study, we were interested in how distinct expectations to an identical auditory stimulus influence the alpha desynchronization pattern in the auditory cortex.1

Among the different kinds of oscillations, those with a frequency between 8 and 12 Hz have received an increasing amount of attention. These so-called alpha oscillations were the first oscillations to be noticed in humans (Berger, 1929) and are ubiquitous in all main sensory and motor brain regions (for a review see e.g., Hari and Salmelin, 1997). They are very prominent in resting EEG and are reduced (‘desynchronized’) as soon as the brain engages in the processing of information (e.g., external input) (Mimura et al., 1962). This has led to the notion that alpha oscillations represent an idling or inactive state of those brain areas in which they are expressed. More recent publications, however, have shown that “idling” is a misleading term. On the contrary, a modulation of alpha oscillations seems to play an essential role in information processing. For example, Tuladhar et al. (2007) showed that alpha activity in occipito-parietal areas increases in a visual working memory task with increasing load. Additionally, alpha oscillations appear to increase in visual areas that are involved in processing distracting information (Thut et al., 2006). Anticipation of a target stimulus leads to a desynchronization of alpha oscillations, which has been demonstrated in the visual (Thut et al., 2006) and somatosensory (Babiloni et al., 2004) areas involved in processing an upcoming stimulus and concomitantly a synchronization of alpha in sensory regions involved in processing a distractor (Rihs et al., 2007, Worden et al., 2000). These findings clearly speak against the conception that alpha is merely an idling rhythm that reflects inactivity. Based on the current knowledge, alpha appears to reflect the excitatory–inhibitory balance within sensory and motor brain regions that can be modulated in a top-down manner (Klimesch et al., 2007, Weisz et al., 2007, Weisz et al., 2011).

In contrast to the visual and somatosensory domains, studies exploring the functional relevance of alpha oscillations in the auditory domain are scarce. This may be related to the fact that auditory alpha activity appears less obvious from resting recordings than, for instance, the dominant visual alpha rhythm (Weisz et al., 2011). Nevertheless, early reports by Lehtelä et al. (1997) and a recent review work by our group (Weisz et al., 2011) clearly demonstrate sound-induced desynchronizations in the alpha range located in the auditory cortex, unequivocally showing that such a rhythm indeed exists in the auditory modality analogous to other modalities. An open question is, however, whether auditory alpha oscillations also have a similar functional role as that reported for the visual or somatosensory systems. To our knowledge, no study exists to date that scrutinizes the relationship between attention towards an auditory stimulus or its saliency and the respective modulations of auditory cortical oscillations. However, some evidence exists that auditory alpha oscillations are involved in auditory memory processes (Pesonen et al., 2006, Van Dijk et al., 2010), in which enhancements were reported that bore striking similarities to findings reported in the visual domain (Tuladhar et al., 2007). These increases during working memory tasks have been interpreted as a disengagement of putatively conflicting regions. So-called top-down effects are normally induced using differing stimuli or by differing the instructions or cues given in an experiment. In the current EEG study, we investigated whether intrinsically fluctuating top-down processes themselves accompany modulations of auditory cortical alpha oscillations. The physical properties of the auditory stimulation were kept constant while the participants' expectancy of whether this tone would be followed by an aversive stimulus fluctuated from trial to trial. Modulation of expectancy was promoted by the fake context of a frequency-discrimination task. Participants were told that they would hear one of two possible tones, each followed by an auditory feedback (aversive noise or silence) after the forced choice (high- vs. low-pitch sound). While the sound actually remained unchanged, the feedback was pseudorandomized according to a procedure shown to modulate expectancy (Perruchet, 1985).

We compared the level of alpha when participants perceived the sound to carry salient information (expectancy of aversive feedback) to instances when the sound was believed to carry non-salient information (expectancy of silent feedback). As most experiments studying conscious perception, the current experiment relies on the subjective report of the participant, in this case which sound was perceived. We are aware of the ongoing discussion in the consciousness literature with regards to the validity of self-reports to reflect veridical contents of conscious perception (Lamme, 2006). Even though debriefings following the experiment are suggestive that participants indeed perceived different pitches associated with differently salient consequences and data by others (e.g., Carrasco et al., 2004) show that expectations can induce modulations of perception equivalent to tuning basic physical properties of a stimulus, from our present study we cannot make statements about the concrete contents of conscious perception when the participants were confronted by the sound. An alternative explanation could be that the subjects' reports were based solely on their expectation of hearing two different sounds which did not influence the concrete perception of the pitch. In short, qualia and their assessment is a highly controversial issue not within the scope of the present study, so when we speak of “perception” then this means “perception reported by the subject” without any strong claims with regards to the accompanying qualia.

Based on findings from the somatosensory modality (Babiloni et al., 2004), we hypothesized that the perception of salient sounds would induce stronger alpha desynchronization in auditory cortical regions. While this is our main hypothesis, we also analyzed our data with respect to possible pre-stimulus effects. Such an effect could not apriori be excluded, as the history of past feedback (i.e., whether salient or not) could have lead to expectations that would have manifested themselves in EEG activity prior to the actual sound onset. We furthermore investigated the period between the onset of perceptual decision and prior to receiving the feedback in order to control for late effects. Although the main focus of this article lies particularly upon possible auditory cortical alpha effects, we also analyzed evoked time-domain measures (the ERP and the slow cortical potentials). Our results show that altered expectations of the same stimulus shape auditory cortical alpha activity during the presentation of the sound; this underscores that the variability of neuronal responses is not necessarily noise but nonetheless carries functionally important information.

Section snippets

Participants

The participants were 16 right-handed, healthy volunteers between the ages of 19 and 27 (mean age ± SD: 22.3 ± 2.35; five men). All participants reported normal hearing and had normal or corrected-to-normal vision. Two participants were excluded from further analysis because of too many artifacts in the EEG data. Two further subjects reported hearing the same tone throughout the experiment and thus were excluded from further analysis (see later). This left 12 participants for the analysis (four

Behavioral task

To achieve sufficient variability in the subjects' expectations of which tone they would hear and thus what feedback was to be expected, we adapted a classical conditioning design by Perruchet (1985) by consecutively presenting the same feedback one to four times. The analysis of the behavioral data of the 14 participants who reported hearing two different tones showed that participants failed to give a response in 2 – 5 trials (mean: 3 trials), resulting in an average of 137 trials that could

Discussion

The aim of the current study was to investigate whether auditory alpha desynchronization elicited by auditory stimulation can be purely modulated by intrinsic top-down mechanisms. The expectation of a (physically not present) high-pitch tone was made salient by associating its occurrence with an aversive consequence (uncomfortable noise). We contrasted trials in which such an expectation occurred with trials in which the participants reported the perception of a low-pitch sound, which was

Acknowledgments

The authors wish to thank Christiane Wolf for her help in acquiring the data. This work was supported by the DFG (grant number WE 4156/2-1).

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