Elsevier

NeuroImage

Volume 47, Issue 2, 15 August 2009, Pages 651-658
NeuroImage

Early gamma-band responses reflect anticipatory top-down modulation in the auditory cortex

https://doi.org/10.1016/j.neuroimage.2009.04.074Get rights and content

Abstract

For efficient and fast encoding of our complex acoustic environment, not only aspects of bottom-up processing are significant, but rather top-down influences such as attention, memory, and anticipation promote specific behavior and perception. Neural oscillatory activity in the gamma-range (30–80 Hz) is discussed as a conceivable candidate to represent very rapid modulations of top-down factors.

We investigated effects of anticipation on early gamma-band responses (GBRs) of the EEG and event-related potentials (ERPs) in response to tone sequences. These sequences were composed of six sinusoidal tones, which could be either regularly ascending or descending in frequency. Thus, the sequences reflected a good continuation of pitch, which also resulted in the buildup of strong expectancies for the upcoming stimulus within the sequence. However, some of the tone sequences contained a violation of the good continuation of pitch at the third or fifth tone position.

The early phase-locked portion of the gamma-band activity was significantly increased when tones were in line with the good continuation of sequences compared to deviant tones. Further, a pronounced early negative ERP response, starting at 150 ms, was elicited by deviant tones at the third and fifth position.

Our results support the notion that gamma-band oscillations reflect perceptual grouping processes of concurrent sounds and anticipatory top-down modulation, which involves some of the first stages of auditory information processing.

Introduction

We live in an extremely complex acoustic environment and are surrounded by simultaneously occurring sounds such as music, speech, and noises from multiple sources. Therefore, it requires a perceptual organization of this extensive mixture of sounds. The auditory system has to segregate and integrate different sounds into meaningful auditory units or objects, which is also known as auditory scene analysis (Bregman, 1994). Bregman (1994) distinguished the perceptual organization along a horizontal (time) and a vertical axis (frequency). The horizontal axis comprises the sequential grouping of sounds over time (e.g. melody), whereas the processing along the vertical axis involves the integration of simultaneous sounds (e.g. forming chords). These grouping processes are governed by both primitive automatic (bottom-up) and learned (top-down) constraints.

Recently, it was suggested that oscillatory activity in the gamma-range (20–80 Hz) is related to bottom-up and top-down factors as well as to the integration of both (Herrmann et al., 2004c). Thus, gamma-band responses (GBRs) might provide additional insights regarding the basic sensory analysis of auditory information as well as the influence of this analysis by top-down processes. Generally, GBRs are divided in an early evoked and a late induced portion. While evoked activity is defined to be time- and phase-locked to an event, induced GBR is time-locked, but shows a high phase variability across trials (Galambos, 1992, Pantev, 1995). Phase-locked oscillatory activity has been reported to be modulated by physical stimulus properties during a very early time interval in the visual (Tzelepi et al., 2000, Bodis-Wollner et al., 2001, Busch et al., 2004, Fründ et al., 2007, Schadow et al., 2007b) and auditory modality (Schadow et al., 2007a, Lenz et al., 2008). The later non-phase-locked GBR between 200 and 400 ms after stimulus onset is mainly associated with a more elaborated processing and is therefore linked to cognitive mechanisms such as attention (Gruber et al., 1999, Tallon-Baudry et al., 2004) and memory (Lutzenberger et al., 2002, Lenz et al., 2007, Busch et al., 2008). However, it has been shown that such top-down modulations can already occur much earlier and can be represented in the evoked gamma-band activity, too. Several visual and auditory experiments have shown an increase in the early evoked activity for target stimuli that capture a higher amount of attention than non-target stimuli (Tiitinen et al., 1993, Herrmann et al., 1999, Debener et al., 2003, Busch et al., 2006). Similarly, the match of a presented stimulus with a memorized template resulted in an enhanced evoked gamma-band response compared to new stimuli (Herrmann et al., 2004d, Busch et al., 2008), which demonstrates a top-down modulation at the earliest stages of information processing. In addition to attention and memory resulting in a faster and more efficient analysis of the upcoming stimulus, most events in everyday life occur predictably for us. Thus, we often anticipate events and are therefore able to prepare a faster and more accurate behavior. Widmann et al. (2007) reported that visual symbolic information affect early auditory sensory processing at 42 ms after tone onset. The authors observed an increase of phase-locked evoked GBR in response to sounds that matched with a corresponding visual symbol and discussed the finding in relation with matching of incoming information against an expectation.

The present study aimed to investigate auditory perception and whether anticipatory processes also result in such early modulation of the auditory evoked GBR. Therefore, we presented regularly ascending and descending tone sequences with six sinusoidal tones. These sequences reflected a good continuation of pitch, which also resulted in the buildup of an expectation for the upcoming stimulus by the listener during the presentation. However, some of the tone sequences contained a violation of the good continuation at the third or fifth tone position. Thus, the sequences violated the listener's expectation at different levels of expectation buildup. Gamma-band activity in response to regularly presented and deviant tones at the third and fifth position of each sequence was compared. If GBRs reflect matching with expectation, responses to regular tones within ascending/descending sequences should be larger than to deviating tones. We assume that regularly occurring tones might be processed by a pretuned population of neurons which is not the case for deviant tones.

Previous research has already revealed electrophysiological correlates of such mechanisms, e.g. the mismatch negativity (MMN), a component of the event-related potential (ERP) after about 150–250 ms (Näätänen, 1992, Näätänen et al., 2007), which is linked to processing of tone sequences and reflects a violation from the preceding stimulus or regularities in complex auditory information (Yabe et al., 2001, Kanoh et al., 2004, van Zuijen et al., 2004, Sussman and Gumenyuk, 2005, Kujala et al., 2007). The MMN operates basically at the sensory memory level and is an automatic process, irrespective of cognitive factors (Schröger, 1997, Näätänen and Winkler, 1999, Schröger et al., 2007). Hence, no behavioral task is needed to elicit a MMN. However, when stimuli are attended for example by a task, then the MMN is partially overlapped by the N2b. The N2b is linked to the expectation of regularly appearing stimuli and indexes deviance detection only if a deviant stimulus is attentively recognized (Näätänen et al., 1982, Novak et al., 1992, Eimer et al., 1996, Rüsseler and Rösler, 2000, Carrión and Bly, 2007). Therefore, we also expected a larger negative ERP response to deviant tones compared to regularly occurring tones within the sequence.

Section snippets

Participants

Seventeen healthy volunteers (9 females, 8 males, mean age 25 ± 3.8 years) participated in the current study. They had no history of hearing impairments and showed no signs of psychiatric or neurological disorders. All participants received a written task instruction and gave informed written consent to participate. They received money or course credits for their participation. The experiment was conducted in accordance with the Declaration of Helsinki.

Stimuli and task

Ten different sinusoidal tones with a

Data acquisition

EEG was recorded with a BrainAmp amplifier (Brain Products, Munich; Germany), using 31 sintered Ag/AgCl electrodes mounted in an elastic cap (Easycap, Falk Minow Services, Munich, Germany). The electrodes were placed according to the 10–10 system, with a nose-tip reference and ground electrode between Fz and Cz. Eye-movement activity was monitored with an electrode placed suborbitally to the right eye. Electrode impedances were kept below 10 kΩ. Data were acquired with a band-pass filter of

Behavioral data

Only trials with responses given between 150 and 2000 ms after the presentation of the red fixation cross were included in the analysis. False trials were excluded from the analysis of reaction times, as well as trials in which the reaction time (RT) exceeded two standard deviations from the mean. On average a number of 30 trials were excluded.

Event-related potentials

In order to test differences in the neural responses to regular and irregular occurring tones, we analyzed amplitudes of the early negativity in the time

Behavioral data

Participants performed the task with high accuracy (ascending sequences: 94% correct, standard deviation (SD) = 6% and descending sequences: 95% correct, SD = 5%). The reaction times to the ascending (441 ms, SD = 87 ms) and descending sequences (447 ms, SD = 97 ms) were nearly identical. Neither the accuracy [t(16) =  0.77, p = 0.455] nor reaction times [t(16) =  1.14, p = 0.271] were significantly influenced by the task.

Event-related potentials

Time courses and scalp topographies of the event-related potentials to regular and

Event-related potentials

The present study showed that irregular sounds within descending or ascending sequences elicited a larger negative deflection in the ERP than regular sounds. The main amplitude difference occurred in a time interval between 150 and 350 ms with an amplitude maximum at posterior scalp electrodes (relative to a nose reference electrode). This early negativity to irregular tones might reflect the ability of the auditory system to extract and apply sequential regularities. Previous research

Acknowledgments

We wish to thank all participants in this study for their time, patience, and effort. The authors would also like to mention the help of Stefanie Thärig, Franziska Bauch, Susanne Fischer, and Stefan Dürschmid during subject recruitment and data acquisition. The study was supported by the German Research Foundation (DFG, Grants HE3353/2-2 and SFB/TR31-A09) and the Honda Research Institute Europe (HRI-EU).

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