Auditory–motor synchronization facilitates attention allocation

Highlights

• ERP oddball experiment with the factors stimulus timing and motor activity

• Larger effect of stimulus timing in the motor condition

• Motor variability correlates negatively with P300 amplitude.

• Motor variability correlates positively with P300 latency.

• Auditory–motor synchronization results in a more efficient attention allocation.

Abstract

Temporal predictability of auditory events induces larger P300 amplitudes and shorter P300 latencies compared to stimulus presentation with variable onset asynchronies. This suggests that periodic stimuli lead to neuronal entrainment resulting in a more efficient allocation of attentional resources. Simultaneous synchronized motor activity should facilitate the precise temporal encoding of acoustic sequences. Therefore the current event-related potential study investigated whether embodied stimulus encoding enhances the reported effects of stimulus periodicity. We found that simultaneous pedaling on an ergometer compared to a physically passive situation amplified the predictability effect on the P300 component. Furthermore, the temporal variability of cycling behavior correlated positively with both P300 latency and P300 amplitude. These findings indicate that auditory–motor synchronization enhances the attentional processing of periodical auditory stimuli.

Introduction

According to the influential dynamic attending theory, neural oscillations “are capable of entraining to external events and targeting attentional energy to expected points in time” (Large and Jones, 1999). The synchronization of internal attending activity with an external event is a prerequisite of attentive processing (Jones et al., 2002). Accuracy should be greatest when the peak of the attentional pulse coincides with the onset of the relevant event. Indeed it has been shown repeatedly that temporally regularly presented stimuli attract attention and are processed faster and more accurately (Correa et al., 2006, Drake et al., 2000, Jones et al., 2002, Rohenkohl et al., 2011). Hence, stimulus periodicity facilitates the focusing of attention on anticipated points in time, resulting in a more efficient allocation of cognitive resources.

Within the last decade several studies have investigated the influence of stimulus periodicity on processing efficiency as reflected by event-related potentials (ERPs), in particular the P300 component. While the ontology of the P300 is still unknown, Polich (2007) has defined the P300 effect as an index of attentional and memory processing. A larger P300 amplitude should indicate the increased allocation of attentional resources, and the P300 latency should indicate how rapidly attentional resources are allocated. Larger P300 amplitudes and shorter P300 latencies should hence reflect successful memory storage facilitating retrieval and recognition.

Recent electrophysiological studies on the effect of stimulus periodicity on attentive processing have corroborated the findings of the above-mentioned behavioral studies by showing that the P300 is sensitive to the temporal regularity of the presented stimuli (Correa and Nobre, 2008, Lange, 2010, Lange, 2009). Schmidt-Kassow et al. (2009) reported better performance as well as a larger P300 amplitude and shorter peak latency in response to periodically compared to randomly presented tones. Stefanics et al. (2010) showed that attended events presented at time intervals corresponding to the delta frequency range (~ 1 s) led to entrainment of delta oscillations resulting in faster stimulus processing. Schwartze et al. (2011) have recently provided evidence for an attentional modulation of the effects of stimulus timing on ERPs. Comparing pre-attentive and attention-dependent temporal processing within the same paradigm, they found that stimulus regularity affected attention-dependent components such as the P3b but not pre-attentional components such as the MMN. This result emphasized the interaction between temporal stimulation properties and the allocation of attention during stimulus encoding. At the same time it underscored the value of the P300 as a reliable tool to investigate stimulus-driven attention.

The current experiment assessed whether the effect of stimulus periodicity on stimulus-driven attention can be amplified by embodied stimulus encoding. People spontaneously coordinate motor activity with periodic auditory sequences via head nodding, finger flipping, or foot tapping, and in turn motor activity guides auditory processing (Drake et al., 2000, Phillips-Silver and Trainor, 2007, Phillips-Silver and Trainor, 2005). We hypothesized that an embodied rhythm leads to an even more precise temporal encoding of the presented stimuli compared to sitting still during encoding. Recently, Su and Poeppel (2012) have shown that body movement actively assisted the extraction of temporal structures in auditory events. In line with this finding, previous neuropsychological studies on rhythm perception have provided evidence for the involvement of motor areas in the perception of auditory rhythms (Bengtsson et al., 2009, Chen et al., 2008, Grahn and Brett, 2007). Moreover there is substantial evidence for a common timing mechanism underlying both perception and production of time intervals (Fraisse, 1982, Ivry and Hazeltine, 1995, Keele et al., 1985, Treisman et al., 1994). Besides, motor activity in response to auditory stimuli is modulated by the way people attend to the stimuli (Jones and Boltz, 1989, Jones et al., 1993, Klapp et al., 1985). Based on this evidence Drake et al. (2000) stated that attentional synchrony can be reflected by motor synchrony. We thus inferred that motor synchrony in turn should result in attentional synchrony, i.e. the more accurately motor performance is timed, the more efficiently can attentional resources be employed for task performance.

Here, we used an auditory oddball paradigm to assess whether auditory–motor interaction may amplify the effect of temporal regularity on stimulus encoding. Participants listened to periodic and aperiodic continuous tone sequences and were asked to silently count deviant tones that differed in sound frequency from the standard tones. They did so a) during a physically inactive control condition and b) while pedaling on a cycling ergometer at very low intensity. The latter condition should lead to an even more efficient allocation of attentional resources, facilitating the temporal encoding of the auditory sequence and deviant processing. In the pedaling condition, we monitored the individual variability of auditory–motor synchronization as a possible further determinant of successful attention allocation and stimulus processing.

We hypothesized (1) decreased P300 latency and increased P300 amplitude in response to periodic compared with aperiodic stimuli. This effect should be modulated by auditory–motor synchronization resulting in stronger timing effects for the auditory–motor condition. (2) P300 latency and P300 amplitude should vary as a function of motor variability. Cycling variability was expected to correlate positively with P300 latency and negatively with P300 amplitude.