Elsevier

NeuroImage

Volume 139, 1 October 2016, Pages 211-217
NeuroImage

Actively but not passively synchronized motor activity amplifies predictive timing

https://doi.org/10.1016/j.neuroimage.2016.06.033Get rights and content

Abstract

Previous studies have shown that the effect of temporal predictability of presented stimuli on attention allocation is enhanced by auditory-motor synchronization (AMS). The present P300 event-related potential study (N = 20) investigated whether this enhancement depends on the process of actively synchronizing one's motor output with the acoustic input or whether a passive state of auditory-motor synchrony elicits the same effect. Participants silently counted frequency deviants in sequences of pure tones either during a physically inactive control condition or while pedaling on a cycling ergometer. Tones were presented either at fixed or variable intervals. In addition to the pedaling conditions with fixed or variable stimulation, there was a third condition in which stimuli were adaptively presented in sync with the participants' spontaneous pedaling. We replicated the P300 enhancement for fixed versus variable stimulation and the amplification of this effect by AMS. Synchronization performance correlated positively with P300 amplitude in the fixed stimulation condition. Most interestingly, P300 amplitude was significantly reduced for the passive synchronization condition by adaptive stimulus presentation as compared to the fixed stimulation condition. For the first time we thus provide evidence that it is not the passive state of (even perfect) auditory-motor synchrony that facilitates attention allocation during AMS but rather the active process of synchronizing one's movements with external stimuli.

Introduction

It is always fascinating to see that acoustic rhythms can incite people to spontaneously coordinate motor activity with auditory sequences via head nodding, finger flipping, hand clapping, foot tapping, or even dancing. This coordination of rhythmic movement with an external auditory rhythm is also called auditory-motor synchronization (AMS). In the current work we investigated how AMS may determine the allocation of attentional resources for predictive timing. As temporally predictably presented stimuli attract attention (Lawrence and Klein, 2013), single events are processed faster and more accurately (Drake et al., 2000, Jones et al., 2002, Correa et al., 2006, Rohenkohl et al., 2011). Thus, temporal regularity facilitates the focusing of attention on anticipated points in time and hence predictive timing results in a more efficient allocation of cognitive resources. The term “predictive timing” is defined as an extension of the notion of predictive coding to the exploitation of temporal regularities (such as a beat) to infer the occurrence of future sensory events (Arnal and Giraud, 2012).

There is increasing evidence that stimulus predictability affects attentive processing (Morillon and Barbot, 2013, Calderone et al., 2014), auditory scene analysis (Bendixen, 2014), and the processing of sensory information (Rohenkohl et al., 2012, Cravo et al., 2013) and that it accelerates reaction times (Stefanics et al., 2010). Work from our laboratory has revealed better performance, as well as a larger P300 response in the human event-related potential to periodically compared to randomly presented stimuli (Schmidt-Kassow et al., 2009, Schwartze et al., 2011, Otterbein et al., 2012).

Previously we have shown that pedaling during rhythmic acoustic stimulation increases P300 amplitude to pitch deviants (Schmidt-Kassow et al., 2013). This effect correlated with the temporal precision with which the subjects synchronized their movements to the presented tones. Hence, AMS amplified the effect of stimulus periodicity on the P300 response.

This is in line with other evidence (Phillips-Silver and Trainor, 2005, Phillips-Silver and Trainor, 2007, Su and Poeppel, 2012, Manning and Schutz, 2013) showing that motor activation influences the perception of auditory information (Cirelli et al., 2014) and that rhythmic movements improve the precision of temporal attention and the quality of sensory selection (Morillon et al., 2014). However, in all of the studies on AMS, participants were asked to actively synchronize their motor output with a given auditory beat. In contrast it has never been studied how adaptive stimulus presentation affects neuronal activity compared with fixed stimulus presentation. During adaptive stimulus presentation stimuli are triggered by a motor response. This kind of stimulus presentation results in a passive state of perfect synchronization as participants' motor activity is always in sync with stimulus onset (passive AMS). Fixed stimulus presentation on the other hand requires that participants actively synchronize their motor activity with the stimuli. This active AMS should direct participants' attention towards the temporal structure of the stimuli but will never result in such a perfect state of synchronization as the adaptive paradigm. Here, we compared the effects of active versus passive AMS by applying a 2-tone oddball paradigm where participants were asked to silently count deviant tones in 5 different experimental conditions: 1) fixed stimulus presentation at 1 Hz while subjects were sedentary, 2) temporally variable stimulus presentation while subjects were sedentary, 3) fixed stimulus presentation at 1 Hz while subjects were pedaling, 4) temporally variable stimulus presentation while subjects were pedaling, 5) adaptive stimulus presentation while subjects were pedaling, i.e. stimuli were presented whenever the pedal crossed a certain point.

Section snippets

Participants

26 right-handed undergraduates with unimpaired hearing participated in this study. Due to technical problems, i.e. incomplete recordings or defective contacts at the light barrier, six datasets had to be excluded. The remaining 20 participants (10 females, mean age: 20.63 years, SD = 3.27) did not report any neurological or psychiatric dysfunctions.

The study was approved by the Ethics Committee of the University of Frankfurt Medical Faculty. All participants were aware of the aims of this study

Behavioral data

On average, participants made less than one error per condition (AP: 0.68 errors, SD = 0.95; FP: 0.74 errors, SD = 0.93; VP: 1.32 errors, SD = 1.60; FS: 0.79 errors, SD = 0.86; VS: 0.47 errors, SD = 0.51) indicating that they paid attention to the tone sequences. The omnibus ANOVA revealed neither a significant main effect of timing or setting nor an interaction between timing and setting (all p-values > 0.09).

ERP data

For P300 amplitude the cluster-based permutation procedure revealed the following results.

For the

Discussion

The aim of the present study was to assess the effect of AMS on predictive timing and attentional allocation. Hence, we intended to contribute to the understanding of the mechanism underlying the observed effects of AMS on temporal encoding. While general sensory-motor synchronization paradigms usually require participants to actively synchronize with a given rhythmic stimulus sequence, here we also included a condition where the stimulation was synchronized with the participants' spontaneous

Conclusions

Taken together, the current study contributes to our understanding of how the allocation of attentional resources and the processing of auditory stimuli can be affected by the perception of regularities in the temporal structure of auditory events and the simultaneous synchronization of motor responses. For the first time we investigated how neurophysiological activity may change during an adaptive in contrast to a fixed stimulus presentation. The findings not only indicate that attention is

Conflict of interest

The authors declare that they have no competing interest.

Acknowledgements

Dr. Maren Schmidt-Kassow was supported by a grant from the German Research Foundation (DFG SCHM 2693/1-2).

References (36)

  • M. Schmidt-Kassow et al.

    Auditory-motor synchronization facilitates attention allocation

    NeuroImage

    (2013)
  • R.I. Schubotz

    Prediction of external events with our motor system: towards a new framework

    Trends Cogn. Sci.

    (2007)
  • M. Schwartze et al.

    Temporal regularity effects on pre-attentive and attentive processing of deviance

    Biol. Psychol.

    (2011)
  • J.G. Smith et al.

    The effect of Parkinson's disease on time estimation as a function of stimulus duration range and modality

    Brain Cogn.

    (2007)
  • J. Sowinski et al.

    Poor synchronization to the beat may result from deficient auditory-motor mapping

    Neuropsychologia

    (2013)
  • M.J. Allman et al.

    Pathophysiological distortions in time perception and timed performance

    Brain

    (2012)
  • L.H. Arnal

    Predicting “When” Using the Motor system's beta-band oscillations

    Front. Hum. Neurosci.

    (2012)
  • A. Bendixen

    Predictability effects in auditory scene analysis: a review

    Front. Neurosci.

    (2014)
  • Cited by (9)

    • Cognitive effects of rhythmic auditory stimulation in Parkinson's disease: A P300 study

      2019, Brain Research
      Citation Excerpt :

      This was in line with previous findings of the RAS effect which is only investigated during sitting in the elderly (e.g., Kotz et al., 2014). More interestingly, while the enhanced effect of temporal predictability in RAS on the P300 was absent during pedaling, the positive correlation between P300 amplitude and motor stability was the same as found previously in young healthy participants (Conradi et al., 2016; Schmidt-Kassow et al., 2013, 2019). That is, the more the motor activity is synchronized with RAS, the higher is the magnitude of P300 amplitudes.

    • Auditory-motor coupling affects phonetic encoding

      2019, Brain Research
      Citation Excerpt :

      While both of these studies separated the EEG recording from the auditory-motor synchronization task, we collected EEG data during auditory-motor synchronization in previous studies. We found that concurrent synchronized motor activity amplifies the timing effect on the P300 (Schmidt-Kassow et al., 2013b; Conradi et al., 2016)., i.e., the P300 was not only enhanced in response to rhythmic as compared to random stimuli, but concurrent motor activity on a stationary bike amplified this timing effect.

    View all citing articles on Scopus
    View full text