Cogn Process (2011) 12:215–218 DOI 10.1007/s10339-011-0391-2

LETTER TO THE EDITOR

Some considerations about the biological appearance of pacing stimuli in visuomotor finger-tapping tasks Irene Ruspantini • Alessandro D’Ausilio Hanna Ma¨ki • Risto J. Ilmoniemi

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Received: 24 November 2010 / Accepted: 11 January 2011 / Published online: 30 January 2011 Ó Marta Olivetti Belardinelli and Springer-Verlag 2011

Abstract Sensorimotor synchronization is a crucial function for human daily activities, which relies on the ability of predicting external events. Synchronization performance, as assessed in finger-tapping (FT) tasks, is characterized by an anticipation tendency, as the tap generally precedes the pacing event. This synchronization error (SE) depends on many factors, in particular on the features of the pacing stimulus. Interest is growing in the facilitation effect that action observation has on motor execution. So far, neuroimaging and neurophysiology studies of motor priming via action observation have mainly employed tasks requiring single action instances. The impact of action observation on motor synchronization to periodic stimuli has not yet been tested; to this aim, a synchronization FT task may be an eligible probing task. The purpose of this study was to characterize a biological pacer at the behavioral level and provide information for those interested in studying the brain processes of continuous observation/execution coupling in timed actions using FT tasks. We evaluated the influence of the biological Electronic supplementary material The online version of this article (doi:10.1007/s10339-011-0391-2) contains supplementary material, which is available to authorized users. I. Ruspantini (&) Systems Biology Technologies Unit, Technologies and Health Department, Istituto Superiore di Sanita`, Viale Regina Elena 299, 00161 Rome, Italy e-mail: [email protected] A. D’Ausilio Robotics, Brain and Cognitive Sciences Department, The Italian Institute of Technology, Genoa, Italy H. Ma¨ki
R. J. Ilmoniemi Department of Biomedical Engineering and Computational Science, Aalto University, Espoo, Finland

appearance of a pacer (a tapping finger) on SE, when compared to an abstract, kinematically equivalent pacer (a tilting hinged bar) and a more standard stimulus (a pulsating dot). We showed that the continuous visual display of a biological pacer yields comparable results to the abstract pacer, and a more robust performance and larger anticipations than a traditional pulsating stimulus. Keywords Sensorimotor synchronization
Visual stimuli
Finger tapping
Stimulus–response similarity

Introduction Human ability to properly coordinate movements with environmental events is fundamental in everyday life. The most striking examples are music and dance performance, which strongly rely on sensorimotor synchronization (SMS). So far, SMS has been mainly investigated in fingertapping tasks, where subjects have to tap in time with a periodic external pacer, e.g., a metronome or a flashing light. Performance is usually evaluated by analyzing the mean value and variability of the synchronization error (SE), i.e., the time lag between the pacer and the tap. A consistent finding is that mean SE is negative (the so-called anticipation tendency): the tap tends to lead the pacing event. This phenomenon emerges very early while tapping; indeed, motor responses get rapidly entrained by predictable stimuli and turn from reactions into anticipations (Repp 2005). SE depends, among many factors, on the physical properties of the pacing stimulus (Aschersleben 2002), such as modality and structure. In fact, synchronization is more accurate with acoustic than visual pacers, as indicated by a lower SE variability (Fraisse 1948; Kolers and

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Brewster 1985; Repp and Penel 2004). Indeed, vision is superior to audition in spatial resolution, but poorer in temporal resolution; this is probably one of the main reasons why audiomotor synchronization is more accurate than visuomotor synchronization (Aschersleben 2002). As for the pacer structure, Buekers et al. (2000) have shown that performance in a visuomotor synchronization task— synchronization of arm movements to a periodic light—is better when the pacer is a moving light travelling back and forth along a horizontal runway than when the pacer is a flashing light alternately appearing at the ends of the runaway. We hypothesize that another pacer feature might be influential in synchronization FT studies: the biological appearance. The perceptual and motor saliency of such stimulus characteristic has been widely demonstrated in different contexts. As an example, it has been shown that human observers exhibit visual sensitivity to species-specific motion (Johansson 1973, Loula et al. 2005). In the last decades, there has been a growing interest in how action observation influences the execution of the same action, giving rise to several cognitive psychology and neuroscience studies. The observation of an action seems to trigger the internal motor representation of the same action, thus priming a motor response and eliciting a spontaneous imitation process. Different cognitive theories have accounted for this mechanism emphasizing the role of a tight perception–action coupling, such as the Gibson’s ecological theory (i.e., the perception of external environment inherently implies information for potential related actions, Gibson 1986) or the ideomotor theory (i.e., action is controlled by the representation of its sensory consequence, Greenwald 1970; Prinz 1990). As Brass et al. (2000) pointed out, the way an action is instructed (e.g., by means of verbal or symbolic instructions or with a direct demonstration) strongly affects the motor performance to follow. In a reaction time task, these authors showed that congruent biological stimuli, when compared with symbolic cues, seem to elicit faster motor responses as if the sensorimotor transformation could benefit from the observation of the same action. On the basis of neurophysiological studies in animal models, it has been hypothesized that a dedicated mirror neuronal system is responsible for the observation/execution matching and might be a precursor of the mechanism by which humans imitate and predict the actions of others (Rizzolatti and Craighero 2004). Iacoboni et al. (1999) suggest that imitation presumably relies on a direct matching of the visual stimulus onto an internal motor representation of that action. So far, this hypothesis has been tested mainly in tasks involving singleinstance, point-to-point movements, such as reaching and grasping.

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On the other hand, FT tasks require a repetitive movement synchronized to an external event. In this case, the relevance of motor salient biological pacers for timed actions becomes more evident if we consider the hypothesis recently proposed by Lewis and Miall (2003) that the motor system is directly involved in time measurements in the sub-second scale. In fact, in this perspective, the biological appearance of a pacer might have an effect on the time representation and, in turn, on SMS. Therefore, we think that FT tasks could become a complementary tool to analyze the impact of biological stimuli in event prediction by means of SE measurements. In order to do this, preliminary tests are needed to characterize pacers with a biological appearance in FT tasks. In the present study, we intend to evaluate motor performance in a visuomotor synchronization task with a biological pacer (a tapping finger) and compare it to the performance elicited by (i) a nonbiological pacer with similar kinematics (a hinged hitting bar) and (ii) a more conventional pacer (a pulsating dot).

Methods Eleven subjects (right-handed; normal or corrected-tonormal vision; mean age 25 years) underwent a fingertapping task with a synchronization paradigm, i.e., to tap their right index finger on the space bar of a PC keyboard in synchrony with a sequence of 63 identical visual stimuli. The three periodic visual cues were presented on a 19’’ PC monitor at a distance of about 70 cm from the subject (resolution: 720 9 540 pixels, size: 21 9 28 cm; visual angle: 33 9 44°). The duration of bar and finger contact with the ground was 40 ms, the same as for the presentation of the dots on the PC monitor. The free extremity of the hinged bar replicated the movement (in terms of amplitude and velocity) of the tip of the tapping finger. The inter-stimulus-onset interval was 800 ms under all conditions. The pacing sequences are available as Supplementary Material in the journal website. Each subject underwent three trial blocks; the three series of stimuli were presented in a random order; a rest period of 3 min was given between trials. To eliminate visual and acoustic feedback from the taps during the tests, the subject’s hand was hidden from sight, and white noise was run through earphones. A custom-made script (Presentation version 11.3, Neurobehavioral Systems, Inc) was used to present the visual stimuli and collect the behavioral data. The first 3 taps in the synchronization phase were discarded from successive analysis to avoid the initial transitional effects.

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absolute values) and lower SE variability when compared with an intermittent pacer. Such an advantage may be explained by the evidence that SE variability decreases when subdivisions are interposed between the pacing events both in the acoustic and visual modality (Repp 2003, 2008). This observation suggests that filling the interstimulus interval (ISI) provides additional temporal references that may elicit a more robust representation of the target interval with a benefit for synchronization. In addition, it may be speculated that Bar and Finger not merely span the whole ISI, but also provide spatial information supplementary to temporal cues, thus augmenting the otherwise limited resources in visual modality for a successful synchronization in time. Buekers et al. (2000) have suggested that the continuous stimuli foster a stronger perception–action coupling. Our results corroborate Bueker’s findings in a synchronization task involving arm movements and extend them to FT tasks, thus suggesting that structured visual stimuli facilitate SMS regardless of the effector used for implementation. From another standpoint, the differences observed in synchronization to continuously displayed versus intermittent visual stimuli may be due to the way the motor response had been instructed, as hypothesized by Brass et al. (2000). In the present study, the Dot is a symbolic cue that only indicates the time at which the tap should end; the stimulus–response association is arbitrary and learned by the subject for the purpose of the experiment. When Bar and Finger are used, the motor response is actually guided by a congruent stimulus. The congruent visual guidance seems to facilitate the motor response, probably relying on a computationally less-demanding visuomotor transformation. This finding is corroborated by neurophysiological evidence, both in animal models (Hoshi and Tanji 2006) and in humans (Toni et al. 2001), that visuomotor processes might follow different computational rules and rely on different cerebral networks, depending on whether the transformation requires a spatially congruent or an arbitrary mapping from stimulus to response. Another interesting result is that Finger and Bar led to equivalent synchronization performances, i.e., the

Table 1 Finger-tapping performance Stimulus

SE mean (ms)

SE SD (ms)

Dot

-8 (5)

47 (1)

Bar

-48 (7)

35 (1)

Finger

-60 (4)

39 (1)

The mean of values and the within-trial variability of the synchronization error (SE) and related standard error of the mean (parentheses) are reported for each condition

SE size and variability were used as measures of the performance outcome.

Results SE mean values and SE variability for the three conditions are shown in Table 1. A one-way repeated-measures analysis of variance (RMANOVA) on the SE mean values reported significant differences between the three pacer conditions (F(2,20) = 16.4, P \ 0.01). Tukey’s HSD follow-up test showed that SE (absolute values, Fig. 1a) was the lowest when the Dot was used (P \ 0.01) and that Bar or Finger pacers did not differently affect the performance (t(10) = 1.79, P \ 0.10). The Dot condition yielded the highest within-trial variability (SD, Fig. 1b) for SE (P \ 0.01), while Bar and Finger pacers induced comparable effects (P = 0.08). It is worth noting that single SE values recorded under the Dot condition were in some cases positive, meaning that the subjects either reacted to or anticipated the synchronization pacer. This phenomenon explains both the lower (absolute) mean SE and the higher uncertainty when synchronizing the tapping with the static intermittent Dot.

Discussion We showed that the continuous display of response-congruent stimuli led to greater anticipation (i.e., greater SE

SE variability

SE mean

A

0

Dot

Bar

Finger

B

– 10

– 40 – 50

40

[ms]

– 30

60 50

– 20

[ms]

Fig. 1 Cue-related differences in synchronization error. Mean SE values are the smallest (P \ 0.01, a) and within-trial variability is the highest under the Dot condition (P \ 0.01, b)

30 20

– 60

10

– 70

0

Dot

Bar

Finger

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observation of a finger tapping was not apparently crucial to further improve SMS. The two pacers probably guide the synchronized tapping in the same way, as they both share a similar kinematics profile and are congruent to the motor response, and may evoke the same internal motor representation. Some neurophysiological and neuroimaging investigations account for such evidence. As an example, studies of biological motion perception have shown that point-light animations of human movement (i.e., image sequences constructed from light points attached to the limbs of an actor) can evoke vivid percept of action [Johansson 1973]. The mirror-neuron-related literature reports that in the macaque, the mirror neurons in premotor cortex specifically respond to real actions (Ferrari et al. 2003), while the human premotor cortex is activated even by the observation of point-light biological motion (Saygin et al. 2004). This difference may be due to a more robust mirror system in humans that can extract a representation of action by motion cues. Indeed, to engage the theorized mirror system, the stimulus should essentially consist of biomechanically possible actions (Romani et al. 2005) and kinematically plausible movements (Casile et al. 2010). Our results are in line with the hypothesis that the mirror mechanism is not modulated by the visual appearance of stimuli, but rather by essential, human-like movement parameters. From a different perspective, the similar effect on SMS performance provides further evidence that the anticipation process may rely on the representation of sequentially structured events, regardless of whether they consist of biological or abstract cues (Schubotz and von Cramon 2004).

Conclusions Here, we showed that using a human tapping finger as a pacer in a visuomotor FT task yields a better performance when compared to the pulsating pacers widely used in SMS studies. We also found that the biological appearance per se is not necessary to facilitate motor responses, as similarly reported in tasks based on point-to-point movements. Therefore, our findings may provide a behavioral baseline evaluation to study the effects of a biological pacer on anticipation processes at the basis of effective SMS. Acknowledgments collection.

We thank Reeta Korhonen for helping in data

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