Action-related auditory ERP attenuation: Paradigms and hypotheses

doi:10.1016/j.brainres.2015.03.038

Brain Research

Volume 1626, 11 November 2015, Pages 54-65

https://doi.org/10.1016/j.brainres.2015.03.038 Get rights and content

Highlights

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Auditory event-related potentials to self-induced sounds are attenuated.
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This may reflect the cancellation of auditory re-afference.
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Or the division of attention between the action and the incoming sound.
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Or the pre-activation of a sensory template upon action–initiation.
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Studies supporting and challenging each account are summarized.

Abstract

A number studies have shown that the auditory N1 event-related potential (ERP) is attenuated when elicited by self-induced or self-generated sounds. Because N1 is a correlate of auditory feature- and event-detection, it was generally assumed that N1-attenuation reflected the cancellation of auditory re-afference, enabled by the internal forward modeling of the predictable sensory consequences of the given action. Focusing on paradigms utilizing non-speech actions, the present review summarizes recent progress on action-related auditory attenuation. Following a critical analysis of the most widely used, contingent paradigm, two further hypotheses on the possible causes of action-related auditory ERP attenuation are presented. The attention hypotheses suggest that auditory ERP attenuation is brought about by a temporary division of attention between the action and the auditory stimulation. The pre-activation hypothesis suggests that the attenuation is caused by the activation of a sensory template during the initiation of the action, which interferes with the incoming stimulation. Although each hypothesis can account for a number of findings, none of them can accommodate the whole spectrum of results. It is suggested that a better understanding of auditory ERP attenuation phenomena could be achieved by systematic investigations of the types of actions, the degree of action–effect contingency, and the temporal characteristics of action–effect contingency representation-buildup and -deactivation.

This article is part of a Special Issue entitled SI: Prediction and Attention.

Introduction

Hearing provides a constant stream of information about the events of the environment. Filtering this flood for relevant pieces of information is enabled by various functions of the human cognitive system. A number of studies show that the auditory system maintains a neural model representing the regularities of the auditory environment (Winkler, 2007, Bendixen et al., 2012), which produces predictions on forthcoming auditory events. These sensory predictions contribute substantially to the information filtering capability of the auditory system by calling capacity-limited (attention and cognitive control) processes only for stimuli which are incompatible with these predictions (Schröger, 1997). Auditory processing can also be influenced voluntarily: one may establish various selective attention sets which allow performing a given auditory tasks more efficiently when the task-relevant sound is presented, while suppressing task-irrelevant auditory input (see e.g. Hillyard et al., 1973, Okamoto et al., 2007). Sounds, however, are not only generated by external sources. We move around, handle objects, talk, and perform various actions, which result in predictable sound events. A number of recent studies suggest that voluntary actions may directly influence auditory processing if the actions result in consistent, predictable patterns of auditory stimulation. These influences are mainly reflected by the attenuation of auditory event-related potentials (ERPs) elicited by such self-induced or self-generated sounds. Such results are generally regarded as fundamental pieces of evidence for theories on speech production (Hickok, 2012), or understanding sensory deficits in schizophrenia (Ford and Mathalon, 2012). The goal of the present review is to summarize recent progress on the measurement and interpretation of action-related auditory ERP attenuation.

Specifically, this review focuses on studies utilizing non-speech-producing actions (mainly finger movements). The main question in this line of research is whether performing the action influences the processing of concurrently (or temporally closely) presented auditory stimuli, and if it does, then what stages of processing are affected and through which mechanisms. Following a technical, non-interpretative description of the paradigm mainly used to address these questions, the typical results and the various hypotheses put forward to explain these findings are presented. Experiments supporting or challenging these hypotheses are presented in the context of the respective hypothesis. The review is concluded by a delineation of outstanding questions.

Section snippets

Measuring auditory processing activity in the presence of on-going action

Measuring auditory processing activity as the participant performs an action is not trivial. In the simplest case, physiological or behavioral responses to sound probes recorded in two conditions are compared: in one condition, the probe is presented concurrently with, in the other in the absence of the given action. Response differences are interpreted as reflections of action-related sound-processing changes.

Depending on the selectivity of the method, such a direct comparison may or may not

Interpreting action-related ERP attenuations

When interpreting the ERP-effects found in contingent paradigms, it has to be kept in mind that some (parts) of the effects may be brought about by the four types of confounds described above. Nonetheless, if the studies manipulate experimental variables for which it can be safely assumed that they are independent from (i.e. they do not modulate) these confounding effects, then the resulting ERP modulations can be readily interpreted as action-related ERP effects.

The common ground of all

Summary and outstanding questions

The studies published in the last couple of years lead to significant advances in the research on action-related auditory ERP attenuation. A number of basic assumptions were confirmed (or at least not rejected), and the set of affected ERP waveforms (and components) was extended.

In addition to the attenuation of the N1 waveform, recent studies also reported action-related attenuations of the P2, T-complex, middle latency-, and induced 40 Hz-responses. The results, however, do not show patterns

Acknowledgments

The writing of this review was supported by the Hungarian Scientific Research Fund—OTKA (108783).

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View full text

ReviewAction-related auditory ERP attenuation: Paradigms and hypotheses

Highlights

Abstract

Introduction

Section snippets

Measuring auditory processing activity in the presence of on-going action

Interpreting action-related ERP attenuations

Summary and outstanding questions

Acknowledgments

Hear. Res.

Electroencephalogr. Clin. Neurophysiol.

Int. J. Psychophysiol.

Int. J. Psychophysiol.

Curr. Opin. Neurobiol.

Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

J. Psychiatr. Res.

Int. J. Psychophysiol.

Brain Res. Rev.

J. Neurol. Sci.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Acta Psychol.

Biol. Psychol.

Biol. Psychol.

NeuroImage

Electroencephalogr. Clin. Neurophysiol.

Biol. Psychol.

Hear. Res.

Neural Netw.

Biol. Psychol.

Acta Psychol.

Biol. Psychol.

Clin. Neurophysiol.

Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Neuropsychologia

Int. J. Psychophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol./Evoked Potentials Section

Curr. Opin. Neurobiol.

Separability of different negative components of the event-related potential associated with auditory stimulus processing

Psychophysiology

Motor-induced suppression of the auditory cortex

J. Cogn. Neurosci.

Selective suppression of self-initiated sounds in an auditory stream: an ERP study

Psychophysiology

Attenuated human auditory middle latency response and evoked 40-Hz response to self-initiated sounds

Eur. J. Neurosci.

Stapedius reflex and monaural masking

Acta Otolaryngol.

Active inference, attention, and motor preparation

Front. Psychol.

A new look at sensory attenuation: action–effect anticipation affects sensitivity, not response bias

Psychol. Sci.

Acoustic and nonacoustic factors modifying middle-ear muscle activity in waking cats

J. Neurophysiol.

Corollary discharge across the animal kingdom

Nat. Rev. Neurosci.

How actions alter sensory processing: reafference in the vestibular system

Ann. N.Y. Acad. Sci.

Electrical reactions of the human brain to auditory stimulation during sleep

J. Neurophysiol.

Acoustic relations of the human vertex potential

J. Acoust. Soc. Am.

Use of partial stimulus information in response processing

J. Exp. Psychol. Hum. Percept.

The updating of the representation of visual space in parietal cortex by intended eye movements

Science

The lateralized readiness potential as an on-line measure of central response activation processes

Behav. Res. Methods Instrum. Comput.

Magnetic auditory responses from the human brain a preliminary report

Scand. Audiol.

Review
Action-related auditory ERP attenuation: Paradigms and hypotheses