The functional significance of the skilled performance positivity: An update

INTPSY-11004; No of Pages 10 International Journal of Psychophysiology xxx (2015) xxx–xxx

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International Journal of Psychophysiology journal homepage: www.elsevier.com/locate/ijpsycho

The functional significance of the skilled performance positivity: An update Hiroaki Masaki a,⁎, Lu Xu a,b, Naoya Taima a, Timothy I. Murphy c a b c

Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan Department of Psychology, Brock University, St. Catharines, ON L2S 3A1, Canada

a r t i c l e

i n f o

Article history: Received 28 March 2015 Received in revised form 13 June 2015 Accepted 15 June 2015 Available online xxxx Keywords: Skilled performance positivity Feedback-related negativity P300 Performance monitoring Error-related negativity

a b s t r a c t The skilled performance positivity (SPP) emerges approximately 450 ms after button presses in a skilled performance task (SPT) where the participant is required to initiate a visual sweep with a left-hand button press and then stop it with a right-hand button press within a predetermined time frame (ranging from 40 to 60 ms). The SPP has been thought to represent appraisal of performance results independent of the reafferent activity, and reported to reduce in amplitude following inaccurate timing performance. We hypothesized that reduced SPP on incorrect trials merely indicates superimposition of the feedback-related negativity (FRN) that is elicited by negative outcomes, because the right-hand button press not only stops the visual sweep but also presents visual feedback. Further, we assumed that the SPP essentially represents a P300 elicited by the visual feedback. To address these questions, we compared the SPT condition and a delayed-feedback (DFB) condition where feedback was presented approximately 1 s after the left-hand button press. We observed the SPP only in the SPT condition, and found feedback-elicited P300s in the DFB condition. Both of these positivities shared a similar scalp distribution. We also replicated the reduced SPP on incorrect trials that shared a similar topography with the FRN elicited by the negative feedback. According to these findings, it is reasonable to conclude that the SPP represents the feedback-elicited P300, and after incorrect performance an FRN is superimposed on it. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Understanding the mechanisms involved in our ability to modify actions based on feedback is critical if we are to gain a more comprehensive understanding of how experience leads to behavior modification. Research done over the past several years has conceptualized the process that initiates remedial actions when we commit errors as performance monitoring (e.g., Ullsperger and von Cramon, 2001). However, some older neurophysiological findings cannot be reconciled with this contemporary perspective of performance monitoring. A reexamination of this earlier research is required periodically to determine not only how these older findings differ from current theories but also how the discrepancies occurred and then reconcile these earlier and more contemporary findings in order to provide a thorough and coherent theory. This process is essential if we are to explain the mechanisms and provide a basis for creating comprehensive new hypotheses as we move forward. One such finding in need of clarification is the skilled performance positivity (SPP) (Papakostopoulos, 1978). The SPP is a positive component following the movement-related cortical potentials (MRCPs) ⁎ Corresponding author. E-mail address: [email protected] (H. Masaki).

including Bereitschaftspotential (BP) (Kornhuber and Deecke, 1965; Vaughan et al., 1968) and a large positive deflection that is referred to as the P2 (Vaughan et al., 1968), reafferent potential (RAP) (Kornhuber and Deecke, 1965), or P+300 (Shibasaki et al., 1980), representing sensory feedback processing (Satow et al., 2004). The SPP can be recorded during a skilled performance task (SPT) where the participant is required to initiate a visual sweep of a target on an oscilloscope with a left-hand button press and then stop it with a right-hand button press within a predetermined time frame (typically ranging from 40 to 60 ms) (Papakostopoulos, 1978). The SPP peaks approximately 450 ms after the left-hand button press, and is thought to represent appraisal of performance results (Papakostopoulos, 1980) or control activity following the results of a skilled performance, independent of the reafferent activity (Fattapposta et al., 1996). The SPP emerged in the SPT, but not in a control condition where a simultaneous button press with both hands initiated the sweep but did not stop it (Papakostopoulos, 1978). The interpretation of these results was that knowledge of results (KR) delivered by the right-hand button press was a necessary condition to obtain the SPP, suggesting that the SPP represents appraisal of performance. Importantly, the SPP became larger on correct trials than on incorrect trials (Papakostopoulos, 1978), and was reduced over frontal regions on incorrect trials in children (Chiarenza et al., 1990). Further, larger SPPs associated with highly skilled

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Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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athletes were also reported in shooting (Fattapposta et al., 1996). These studies concluded that amplitude of the SPP is associated with better timing performance, and thus may potentially be a useful index of timing control. However, this interpretation of the SPP remains somewhat doubtful. It is not clear if the SPP is indicative of evaluation of performance outcome or the internal monitoring of performance itself. According to the perspective of performance monitoring, it is more reasonable to interpret that reduced SPP on incorrect trials represents an overlapping of the error-related brain activities on the SPP. It is well-known that a negative-going deflection over frontocentral regions is elicited by feedback indicating that a response was incorrect or signaling a negative outcome that is referred to as the feedback-related negativity (FRN) (Hajcak et al., 2007; Miltner et al., 1997; Yeung and Sanfey, 2004) or the medial frontal negativity (MFN) (Gehring and Willoughby, 2002; Masaki et al., 2006). The FRN has been investigated in association with the error-related negativity (ERN or Ne) that is elicited by erroneous responses, has a maximal amplitude over frontocentral regions (Falkenstein et al., 1991; Gehring et al., 1993) and is presumably generated from the anterior cingulate cortex (ACC) (e.g., Holroyd et al., 1998; Kiehl et al., 2000). Because the FRN elicited by negative feedback is superimposed on the positive deflection following feedback, we suspect that the reduced SPP over frontal regions on incorrect trials reported by previous studies (Papakostopoulos, 1978; Chiarenza et al., 1990) was due to contamination from the FRN. In the SPT, participants receive instantaneous feedback by observing if the target stopped within the predesignated area of the computer monitor, differing from procedures of most FRN studies where participants are not certain of the correctness of their decision or response prior to feedback. It should be pointed out that continuous motor tasks (e. g., tracking movements), presenting participants online feedback similar to the SPT elicit a FRN (e.g., Krigolson and Holroyd, 2006, 2007; Krigolson et al., 2008, 2012). Although participants likely online-monitor a moving target with their own eyes in the SPT, basically they do not recognize performance outcomes until the moving target stops because of its rapid velocity (1 m/s), unless they press the stop button relatively late (i.e., overshoot errors). In addition, they cannot online correct their response using online feedback because the target range is very short (i.e., 20 ms) and thus the motor program must be assembled before the initiation of the task (see Keele, 1968). Thus, the feedback cannot help on-line in a given trial to determine the correct timing because the required response time (i.e., 50 ± 10 ms) is beyond human capability; however it may be used to estimate the required coordination between button presses on future trials. The characteristics also differ from time-estimation tasks used in FRN studies where a relatively longer duration (1 s) is estimated (e.g., Krigolson and Holroyd, 2007; Krigolson et al., 2012; Miltner et al., 1997). Thus, to recognize outcome of an action in the SPT participants rely on externally-presented feedback, probably also due to the visual dominance (e.g., Klein, 1977), and rely less on internal monitoring. The characteristics of the SPT may also raise a question whether participants rely on the internal error monitoring that elicits the “response-locked” ERN rather than the external error monitoring that elicits the FRN. The ERN emerges before the feedback presentation when the ability to infer the outcome of an action is very high because of the utilization of internal information (Heldmann et al., 2008; Luu et al., 2000). If participants use internal monitoring in the SPT, the ERN time-locked to erroneous stopping responses should emerge even without feedback. Alternatively, if the monitoring processes in the SPT are similar to those used in continuous tracking movements, an early negative component (ERN) generated from the frontal error system that assesses high-level errors should be followed by another negative component associated with the posterior error system that assesses low-level errors, representing hierarchical error processing (Krigolson and Holroyd, 2006, 2007). In the SPT, the visual feedback elicits a SPP with the same latency as that of the P300. This comparable timing of the SPP and P300 may be a

potential flaw in the design of the SPT that makes it difficult to differentiate any changes in the SPP from the P300 due to experimental manipulation. If the P300 was misidentified as the SPP in earlier studies, the assertion that the SPP amplitude represents timing skills is incorrect and may have encouraged the motor control research to employ a false research tool. Therefore, a more thorough examination of these phenomena needs to be undertaken to clarify the underlying mechanism for these results. Indeed, Papakostopoulos (1980) compared the SPP and a positive component elicited by externally or self-paced presentations of the visual stimulus. He asserted that the SPP is not a compulsory component of visual-evoked potentials and thus it differs from the P300 because its latency and duration are considerably longer than the visual-evoked positive components (Papakostopoulos, 1980). However, this argument is not convincing, because the visual-evoked potential tested as a control in that study was not driven by performance-outcome, and the original methodology of the SPP used the left-hand button press as the temporal reference, resulting in a longer latency of the positivity that might actually have been triggered by feedback presented at the instance of the right-hand button press. It would be time-locked to the right-hand button press which results in the feedback. Thus, this raises the question that the so-called SPP may actually reflect the feedbackevoked P300 and/or FRN. In the present experiment, we wished to determine if the SPP could be differentiated from the feedback-evoked P300 or if they both represent the same phenomenon. First, we identified the SPP according to the procedure of Papakostopoulos (1980) that compared the SPT with two control conditions. The first control condition replicated the original experiment where a simultaneous button press with both hands was executed (Papakostopoulos, 1978). The other control condition more closely mimicked the motor response in the SPT by pressing the buttons in rapid succession. These control conditions were needed to identify the SPP that diverges from P2. In both control conditions, the righthand button press did not stop the moving sweep initiated by the lefthand button press. We predicted that only the P2 should be observed in these control conditions, whereas the SPP should emerge in the SPT condition in accordance with previous studies of SPP (Fig. 1). To address these hypotheses, we averaged the SPP time-locked to the right-hand

FRN FRN

SPT condition DFB condition Control

P2 + 100 ms

SPP

P300 time

right button press instantaneous feedback

delayed-feedback

Fig. 1. Schematic illustration of the present hypothesis. The black line represents a waveform in the control conditions, red lines represent waveforms in the skilled performance task (SPT) condition, and green lines represent waveforms in the delayed-feedback condition. Solid lines for both the SPT and the delayed-feedback condition represent waveforms on correct trials and dashed lines represent waveforms on incorrect trials. We predicted that only the P2 should be observed in these control conditions, whereas the SPP should emerge in the SPT condition. We also predicted that the SPP should not emerge when the delivery of feedback was delayed, but instead a similar positive deflection to the SPP should be elicited by the delayed-visual feedback. If the reduced SPP on incorrect trials is due to the feedback-related negativity (FRN), the reduced SPP should not be observed in the delayed-feedback condition. We would see the comparable relationship in ERP waveforms between correct and incorrect trials both for SPT (right after right response) and for delayed-feedback condition (right after the delayed-feedback onset).

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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button press, because it would be more synchronized to the right-hand button press and we tested two control conditions that differed in the interval between the right and the left-hand button presses. The second purpose was to test our prediction that the SPP should not emerge when the delivery of feedback was delayed because the SPP represents a feedback-evoked P300, but instead a similar positive deflection to the SPP should be elicited by the delayed-visual feedback (Fig. 1). For this reason, we tested a delayed-feedback (DFB) condition, in which the visual feedback was not delivered with the same timing of the right-hand button press. Thus, it was expected to clearly differentiate the SPP from the P2 in the DFB condition. The third aim of our study was to examine whether the error-related negative components are indeed superimposed on the SPP for incorrect responses that would then result in a reduced SPP (Fig. 1). If the reduced SPP on incorrect trials is due to the FRN, the reduced SPP should not be observed in the DFB condition (meeting the premise of the existence of SPP in this condition), because the visual feedback is not delivered immediately after the right-hand button press. In addition, if the participants rely on their internal monitoring to execute the SPT without feedback (i.e., the DFB condition), the ERN should be elicited by incorrect timing responses (Heldmann et al., 2008; Krigolson et al., 2008; Luu et al., 2000), reducing the SPP amplitudes. More importantly, when comparing the difference waves (incorrect minus correct) of the SPP in the SPT condition and the FRN elicited by the delayed feedback in the DFB condition, we would expect to see comparable amplitudes and scalp topographies in these event-related potentials (ERPs). 2. Materials and methods 2.1. Participants We tested 30 male participants recruited from Waseda University's Faculty of Sport Sciences, aged 19 to 23 years (M ± SD: 20.8 ± 1.1 years), with mean handedness score 76.6 (Oldfield, 1971). Participants had normal or corrected-to-normal vision and were paid 3000 yen (about 30 U.S. dollars) for their participation. Written informed consent was obtained. This study was approved by the Waseda University Ethics Committee.

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instead of an oscilloscope. On each trial a fixation cross was presented in the center of a rectangular task display (97 mm × 75 mm) on an cathode ray tube (CRT) monitor (405 mm × 300 mm, display resolution 1280 dot × 1024 dot, refresh rate 85 Hz, Iiyama, Inc., HM204D-A) that was set 1 m in front of the participant. Participants were instructed to initiate a single sweep of a circle across the rectangular task display by pressing a button with their left thumb and to stop the moving circle within a defined target area (13 mm × 13 mm) of the CRT (i.e., between 40 and 60 ms after initiation) by pressing the other button with their right thumb (Fig. 2). The fixation cross disappeared with the left button press. The response buttons (15 mm × 15 mm) were mounted on a plastic case (125 mm × 180 mm × 35 mm) and 43 mm apart from each other. The sweep velocity was 1 m/s. The sweep circle was yellow in color (6 mm in diameter). For participants' reference, a square that represented the target range was constantly visible in the center of the monitor during the experimental block. Termination of the moving circle within the target area after its initiation was referred to as a correct performance. Thus, the participant recognized his own performance outcome with the termination of the sweep and was immediately aware if the trial was correct. All stimuli were presented by Presentation software (Neurobehavioral Systems, Inc.) on a CRT monitor. 2.2.2. The delayed feedback condition (DFB) The procedure in the delayed feedback (DFB) condition was identical to the SPT except for the timing of the feedback presentation. Although participants initiated a single sweep of a circle by pressing a button with their left thumb and were instructed to press the other button with their right thumb while the moving circle was within the specified area (square on the computer monitor), the moving circle continued moving even after the right thumb press. After the moving circle disappeared at the right edge of the task display, it appeared again from the left edge and continued moving to the right edge of the task display (Fig. 2). During the third consecutive and continuous sweep across the task display, the moving circle stopped at the point where it was when the original right-hand button press had been made (i.e., 910 ms + performance time after the left thumb press). This was done to dissociate any electrocortical responses due to the right-hand button press from those associated with the visual feedback indicating if the trial has been successful or not.

2.2. Tasks 2.2.1. The skilled performance task (SPT) We adopted a modified SPT using commercially available stimulus presentation software (Presentation, Neurobehavioral Systems, Inc.)

2.2.3. Control After participants initiated a single sweep of a circle by pressing the button with their left thumb, the yellow circle did not stop regardless of the right-hand button press. We tested two control tasks. The first was

Fig. 2. Schematic illustration of the skilled performance task (SPT) procedure in the delayed feedback condition. Each trial began with presentation of a fixation cross. Participants pressed the left button to initiate a sweep circle and pressed the right button to stop it within the target area (i.e., ranging from 40 to 60 ms). The sweep circle stopped with the right button press in the SPT condition (i.e., instantaneous feedback), whereas it stopped on the third consecutive continuous sweep across the task display in the delayed feedback condition (910 ms + performance time after the left thumb press). In the delayed-feedback condition, the interval between the moving circle appearing at the left edge of the task display and the next appearance of the circle at the left edge of the display was 455 ms. The target box remained on the screen for about 200 ms after the moving circle disappeared at the right edge of the screen. (For interpretation of the references to color in this figure, the reader is referred to the web version of this article.)

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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the same as originally employed by Papakostopoulos (1978). Participants were asked to execute a simultaneous button press with both their left and right hands. The presentation software initiated a sweep with the timing of the left-hand button press, but did not stop the sweep. The single sweep disappeared when it reached the right edge of the monitor. We tested this control for the first 12 participants (one participant was excluded from analysis due to excessive EEG artifacts). The other control task was conducted for the remaining 18 participants. In this task, participants were asked to press the left button to initiate a sweep then press the right button; however, the button press did not stop the sweep. The succession and timing of these button presses was encouraged to be similar to the responding manner during the SPT. This second control task allowed us to compare the ERPs in the SPT condition, while keeping the responding manner consistent. In the simultaneous button press control, it is likely that the left-hand button press is technically preceded by the right-hand button press, although participants do not recognize it. Note that only the control tasks varied between two experiments, but both the SPT and the DFB condition were identical between experiments. All three conditions including controls consisted of two blocks (40 trials/block) and were counter balanced within a participant by applying an ABCCBA order (e.g., Control → SPT → DFB → DFB → SPT → Control) to eliminate any sequential effect. Before the experiment began, participants were trained in the procedure of pressing the left, and then right buttons and allowed to practice until they understood the correct responding behavior. Each time a participant started a new condition, he was asked to practice the task (less than 10 trials) to reconfirm adherence to the procedure. 2.3. Electrophysiological measurements 2.3.1. Recording The electroencephalogram (EEG) was recorded from 128 sites with Ag/AgCl electrodes. Horizontal electrooculograms were recorded from the left and right outer canthi, and vertical electrooculograms from above and below the left eye. These signals were recorded, using the Biosemi Active Two system (Biosemi Inc.). Both EEG and EOG signals were digitized at a rate of 1024 Hz (i.e., with a bandwidth of DC to 205 Hz, −3 dB/octave). The electromyograms (EMG) were bipolarly recorded from the flexor pollicis brevis muscles in the left and right palms with Ag/AgCl electrodes using the Biosemi Active Two system (with DC derivation), and were off-line high-pass filtered with 5.31 Hz, full-wave rectified, and low-passed filtered with 30 Hz with the Vision Analyzer (Brain Products). 2.3.2. Data analysis Processing of EEG was performed with the software package Brain Vision Analyzer (Brain Products). The EEG was re-calculated to an average reference and corrected for ocular movement artifacts using the procedure described by Gratton et al. (1983). We averaged SPPs using the right-hand button press as a trigger. Trials in which the interval between the left and the right-hand button presses exceeded 200 ms were excluded from ERP averaging to avoid contamination of medial frontal activities signaled by a second type of external feedback (disappearance of a sweep). Trials where the EEG amplitude exceeded a threshold of ±100 μV during the recording epoch in every electrode were also excluded. ERPs were bandpass-filtered with DC to 30 Hz (roll-off 24 dB). SPP averaged using the right-hand button press as a trigger was measured within a window of 200 to 500 ms after the right-hand response relative to the pre-response baseline (i.e., mean amplitude between −200 to −100 ms before the right-hand button press). Further, to investigate any difference in SPP amplitudes in terms of performance correctness, we averaged SPPs time-locked to the right-hand button press separately for correct and incorrect trials. To obtain FRN and P300, we averaged the feedback-elicited ERPs separately for correct and incorrect trials as well as the feedback-elicited ERPs including both correct and

incorrect trials. Because the order of conditions was counterbalanced in this study, any possible effect of more incorrect responses made in the beginning of the task influencing the results was minimized. For the analyses in Section 3.4, the feedback-elicited ERP amplitudes were measured within a window of 200 to 500 ms after the delayedfeedback relative to the pre-stimulus baseline (mean amplitude ranging from −100 to 0 ms). Behavioral data were tested using a mixed two-way ANOVA with repeated measures on condition (SPT/DFB), including a group factor (simultaneous/sequential control). SPP amplitudes were tested using a mixed three-way ANOVA with a group factor and repeated measures on condition (control/SPT/DFB) and electrode (Fz/FCz/Cz/Pz). To compare correct and incorrect trials, SPP amplitudes were tested using a mixed four-way ANOVA with a group factor and repeated measures on correctness (correct/incorrect), condition (SPT/DFB), and electrode (Fz/FCz/Cz/Pz). Where post hoc comparisons were required, the Bonferroni correction was applied. We reported the Greenhouse– Geisser epsilon value along with the original degrees of freedom and if the assumption of sphericity was violated the adjusted significance level (p value). 3. Results 3.1. Performance The rate of correct responses did not differ between the two groups (F(1, 27) b .1, p = .94, pη2 b .01). It revealed better performance in the SPT (M = 57%, SEM = 2.3) than in the DFB (M = 48%, SEM = 2.1) condition (F(1, 27) = 17.7, p b .01, pη2 = .40). No interaction was found (F(1, 27) b .1, p = .98, pη2 b .01). Overall response time did not differ between the two groups (F(1, 27) = 1.8, p = .19, pη2 = .06). It was significantly longer for the DFB (M = 59 ms, SEM = 1.7) condition than for the SPT (M = 55 ms, SEM = 1.0) condition (F(1, 27) = 6.1, p = .02, pη2 = .19). No interaction was found (F(1, 27) = .9, p = .35, pη2 = .03). 3.2. Skilled performance positivity Fig. 3 shows positive deflections following the right-hand button press. Obviously, SPPs developed during the SPT regardless of the type of control condition; however, the SPP did not appear in the DFB condition even though participants performed a skilled performance task. Fig. 3 also shows the topographies of SPP for both types of control. Regardless of the control condition, the SPP showed a central focus. Fig. 3 also shows a feedback-evoked ERP in the DFB condition more than one second after the right-hand response. To compare mean amplitudes ranging from 200 to 500 ms after the right-hand response across conditions (Fig. 4), a mixed 3-way ANOVA was conducted. There was no significant difference between the two groups (F(1, 27) = 1.7, p = .20, pη2 = .06). Main effects of both condition (F(2, 54) = 47.5, p b .01, pη2 = .64) and electrode (F(3, 81) = 26.4, p b .01, ε = .65, pη2 = .49) were obtained. An interaction of condition and electrode was also obtained (F(6, 162) = 13.5, p b .01, ε = .59, pη2 = .33).1 The positivity was significantly larger in the SPT condition 1 We also examined SPPs time-locked to the left response (mean amplitudes ranging from 300 to 600 ms following the left response using a pre-response baseline) that had been used in previous SPP studies. Although similar results were obtained, F-values were in general smaller relative to the results of SPP time-locked to the right response, suggesting that SPP may be more time-locked to the right response that provided feedback. Although there was no difference between the two groups (F(1, 27) = .8, p = .37, pη2 = .03), both main effects of condition (F(2, 54) = 40.5, p b .01, pη2 = .60) and electrode (F(3, 81) = 25.6, p b .01, ε = .68, pη2 = .49) were obtained. An interaction of condition and electrode was also obtained (F(6, 162) = 11.0, p b .01, ε = .57, pη2 = .29). These interactions were primarily due to larger positivities in the SPT than in the other two conditions except over Fz. These results resembled the results of SPPs time-locked to the right response.

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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Fig. 3. Grand averaged waveforms of the SPPs for the simultaneous button-press group (left panel) and for the sequential button-press group (right panel). The vertical dotted lines represent the right-hand response onset. Only the skilled performance task (SPT) elicited the SPP. In the delayed-feedback condition (DFB), P300s elicited by the delayed feedback were observed instead of the SPP. The SPPs in the SPT condition for both control groups showed a central focus. Two topographical maps represent activities ranging from 200 to 501 ms following the right button press.

than in the other two conditions at FCz, Cz, and Pz (all comparisons: p b .01), but not at Fz. The positivity was significantly larger at Cz than at Fz and Pz, and larger at FCz than at Fz in all conditions (all

comparisons: p b .01). However, in the SPT condition the positivity was also larger at Pz than at Fz (p = .01) and larger at Cz than at FCz (p = .04).

Fig. 4. Mean amplitudes of the SPP ranging from 200 to 500 ms following the right-hand button press.

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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3.3. Comparison between correct and incorrect trials In order to determine if the FRN is superimposed on the SPP on incorrect trials, we also compared the SPT and the DFB conditions in terms of correctness. Performance results suggested that the two different controls did not influence performance. Thus, to investigate the effect of correctness on SPP, we re-averaged post-movement positivities time-locked to the right-hand button press separately for correct and incorrect trials, including both control groups (Fig. 5). For this analysis, one participant was further excluded from the simultaneous-control group due to a low number of correct trials in the SPT condition (total 10 participants for this group). We did not exclude this participant in Section 3.2, because the differentiation between correct and incorrect trials was not essential to address the first two purposes of this study according to previous SPP studies. As can be seen in Fig. 3 (left panel), in the SPT condition, a negative deflection was observed over frontocentral regions (maximum at FCz) on incorrect trials about 200– 350 ms after the right-hand button press. However, in the DFB condition (Fig. 5 right panel), neither SPP nor negative deflection was observed. Instead, positive deflections were elicited by the delayed-feedback presentation. Importantly, positivity elicited by the delayed-feedback was smaller on incorrect trials due to superimposition of a negative component (see more details in Section 3.4). To support these observations, a mixed 4-way ANOVA conducted on mean amplitudes ranging from 200 to 500 ms following the right-hand button press (Fig. 6) revealed no group effect (F(1, 26) = .7, p = .40, pη2 = .03), but main effects of correctness (F(1, 26) = 7.3, p = .01, pη2 = .22), condition (F(1, 26) = 67.4, p b .01, pη2 = .72), and electrode

Fig. 6. Mean amplitudes of the post-movement positivity ranging from 200 to 500 ms after the right-hand response on correct and incorrect trials both in the SPT and DFB conditions.

(F(3, 78) = 23.6, p b .01, ε = .65, pη2 = .48). In addition, a significant interaction between correctness and condition was found (F(1, 26) = 8.4, p = .01, pη2 = .24). Reduced positivity (or more negativity) on incorrect trials was observed in the SPT condition (p b .01), but not in the DFB condition (p = 1.00). A significant interaction of correctness and electrode was also observed (F(3, 78) = 6.8, p = .01, ε = .52, pη2 = .21). The amplitudes were significantly less positive on incorrect trials than on correct trials over frontocentral regions (Fz: p = .01, FCz: p b .01, Cz: p = .04) but not over the parietal region (Pz: p = .24). In

Fig. 5. Left panel: SPP waveforms time-locked to the right-hand button press in the SPT condition for correct and incorrect trials (N = 28). Right panel: post-response positivities in the DFB condition for correct and incorrect trials. Green lines represent difference waves calculated by subtracting correct trials from incorrect trials. The topography of different wave (ranging from 200 to 300 ms) in the SPT condition reveals a frontocentral distribution of incorrect-related negativity.

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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addition to a pattern of larger positivity at FCz and Cz than at Fz and Pz (all comparisons: p b .01) that was found for both correct and incorrect trials, a larger positivity at Pz than at Fz was observed for incorrect trials. Furthermore, a significant interaction of condition and electrode was obtained (F(3, 78) = 11.8, p b .01, ε = .75, pη2 = .31). This interaction reflects virtually identical results as the above-mentioned interaction between condition and electrode (Section 3.2) except that there was no significant difference between Cz and FCz in the SPT condition (p = .06). However, we also obtained an interaction among group, correctness, and electrodes (F(3, 78) = 5.3, p = .01, ε = .52, pη2 = .17). Post-hoc tests revealed that a tendency of more negativity on incorrect than on correct trials was not observed at Cz for the simultaneous control

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group (p = .39) and was marginally significant at FCz for the sequence control group (p = .05). 3.4. Feedback-related ERPs in the DFB condition Fig. 7 (left panel) shows the feedback-elicited ERP in the DFB condition, including both correct and incorrect trials. The delayed feedback elicited a P300 with a central focus. Fig. 7 (right panel) shows the ERP waveforms elicited by the delayed feedback on both correct and incorrect trials. The delayed feedback elicited a negative deflection on incorrect trials in the DFB condition. In addition, topography of the difference waveform (incorrect minus correct trials) shows a maximum amplitude at FCz. We compared mean amplitudes ranging from 200 to 500 ms

Fig. 7. Left panel: the feedback-elicited ERP waveforms including both correct and incorrect outcomes. The topography shows the scalp distribution of feedback-elicited positivity (ranging from 200 to 500 ms after the feedback). Right panel: the feedback-elicited ERPs for correct and incorrect trials. Green lines represent the difference waves obtained by subtracting correct trials from incorrect trials. The topography of the different wave (ranging from 200 to 300 ms) is also shown at the top of the panels.

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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Fig. 8. Mean amplitudes (ranging from 200 to 500 ms) of the SPP in the SPT condition and of the feedback-elicited ERP in the DFB condition on correct and incorrect trials.

after the delayed-feedback onset (Fig. 8) with mean amplitudes ranging from 200 to 500 ms after the instantaneous feedback onset (i.e., righthand response) in the SPT condition on both correct and incorrect trials. A mixed 4-way ANOVA revealed no difference between the two groups (F(1, 26) b .1, p = .95, pη2 b .01). It confirmed more negative amplitudes on incorrect trials than on correct trials (F(1, 26) = 24.2, p b .01, pη2 = .48), smaller amplitudes in the DFB (i.e., feedback-ERPs) than in the SPT condition (F(1, 26) = 58.6, p b .01, pη2 = .69), and a main effect of electrode (F(3, 78) = 24.8, p b .01, ε = .66, pη2 = .49). An interaction between correctness and electrode was also found (F(3, 78) = 4.7, p = .01, ε = .66, pη2 = .15), indicating that more negative amplitudes were found over frontocentral regions for incorrect trials (all p's b .01), but not at Pz (p = .38). The positivity was smaller at FCz than at Cz on incorrect trials (p = .03). Although an interaction of condition and correctness was not obtained (F(1, 26) = .4, p = .51, pη2 = .02), an interaction of condition and electrode was found (F(3, 78) = 4.4, p = .02, ε = .58, pη2 = .14), indicating smaller amplitudes of feedbackelicited ERPs in the DFB than SPPs in the SPT condition for Pz, Cz and FCz (all p's b .01); however this difference was not significant at Fz (p = .06). In addition, the positivity was larger at Pz than at Fz only in the SPT condition (p = .02). 4. Discussion In the present study, we attempted to clarify the functional significance of the SPP. The main findings were that (1) the SPP was obtained in our modified SPT in either simultaneous or sequential control task, (2) the SPP associated with the right-hand response emerged in the SPT condition, but not in the DFB or the control conditions, (3) the SPP was replaced by the feedback-elicited P300, peaking more than one second after the right-hand response, in the DFB condition, and (4) a negative deflection appeared to be superimposed on both the SPP and the feedback-evoked P300 on incorrect trials with the same latency relative to the eliciting-event (i.e., 250 to 300 ms). In terms of performance, response accuracy in the SPT and DFB condition was not influenced by the different control tasks, whereas it was significantly higher in the SPT than in the DFB condition. To identify the SPP, we tested two different control conditions where the sweep was not stopped by the second button press. Indeed, we identified the SPP following the P2 in the SPT condition regardless of the control condition. To clarify the functional significance of SPP, we evaluated brain activities associated with motor timing control and visual-feedback processing separately in the DFB condition. The results clearly showed that the SPP was not observed in the DFB condition. This result does not support the notion that the SPP can represent internal performance monitoring (Luu et al., 2000; Heldmann et al., 2008), because it should have emerged immediately after the right-hand

response even in the DFB condition. In general, our results supported the hypothesis that if the SPP is actually a feedback-evoked P300, there should be no SPP immediately after the right-hand response but that there would be a similar morphology associated with the SPP elicited by the delayed visual feedback. Papakostopoulos (1980) did not obtain the SPP using similar procedures to our delayed feedback condition, because he tested this ad-hoc procedure for only two individuals and did not present knowledge of results (KR) after they pressed the right-hand button. In our study, the delayed feedback that was not used in previous studies did elicit a positive deflection similar to the SPP. The temporal shift of positivity observed in the delayed-feedback procedure provides evidence that the SPP is actually a positivity elicited by feedback. This is not in conflict with the assertion of Papakostopoulos (1980) that the SPP might be related to appraisal or knowledge of performance result. However, we assert that the SPP is actually a P300 similar to those reported in studies that adopted tasks where feedback was given to participants (e.g., Hajcak et al., 2007; Wu and Zhou, 2009; Yeung and Sanfey, 2004; Zhou et al., 2010). Chiarenza et al. (1990) also suggested that SPP is a similar component to the P300 because its latency seemed to depend on the evaluation time of the feedback information in accordance with earlier P300 studies (e.g., Kutas et al., 1977). A similar possibility that P300 may be superimposed on the preceding P2 was also suggested in an earlier study (McAdam and Rubin, 1971). We also examined whether the FRN was superimposed on the SPP after incorrect trials, resulting in a reduced SPP. We clearly found an FRN elicited by the delayed feedback signal when we compared correct and incorrect trials. We also compared SPPs between correct and incorrect trials. Previous studies found reduced SPP on incorrect trials (Chiarenza et al., 1990) or larger SPP associated with correct performance (Fattapposta et al., 1996), suggesting that SPP might be indicative of performance control. We found that the SPP showed different waveforms between correct and incorrect trials in the SPT condition, although the SPP itself did not emerge in the DFB condition. The SPP was significantly reduced during the same time window as the FRN. Importantly, the negative deflections on incorrect trials that were superimposed on both the SPP and P300 elicited by the delayed feedback shared the same scalp distribution (i.e., maximal at FCz). In terms of topography, latency, morphology, and ERP characteristics on incorrect trials, it is reasonable to conclude that the SPP following the P2 represents a P300 elicited by feedback that is associated with KR to participants. It is difficult to unequivocally regard two ERPs as identical components simply based on observations; however, the similarities between the SPP and P300 appears to meet the criteria to identify ERP components (Coles and Rugg, 1995) suggesting that both are very similar. These criteria were also used to support the assertion that the ERP waveform associated with negative feedback was similar to the N200 (Holroyd et al., 2008). Previous studies have examined the SPP in children (Chiarenza et al., 1990), athletes who were highly trained in a sport (Fattapposta et al., 1996; Fontani et al., 2007), patients with Parkinson's disease (Fattapposta et al., 2002) and children with dyslexia (Chiarenza, 1990; Chiarenza et al., 2014), because it has been thought to reflect evaluation of performance results (Papakostopoulos, 1980). In other words, the SPP is related to evaluation of a motor action (Fontani et al., 2007). Our results also support the account of appraisal of performance. However, previous studies have evaluated both the P2 that reflects reafferent activity and P300 elicited by feedback as similar positivities. This is not appropriate if the goal is to purely evaluate the appraisal process of participants. It may be even more critical to have an accurate theoretical model if the SPP may be used as a clinical tool (e.g., Chiarenza, 1990; Fattapposta et al., 2002). We dissociated between the P2 and SPP with the delayed feedback procedure. Therefore, the feedback-elicited potentials may be a more valid index to evaluate appraisal processes, as long as the responserelated positivity (P2) and the SPP can be dissociated. This paradigm

Please cite this article as: Masaki, H., et al., The functional significance of the skilled performance positivity: An update, Int. J. Psychophysiol. (2015), http://dx.doi.org/10.1016/j.ijpsycho.2015.06.007

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provides a theoretical advantage in the interpretation of the results without limiting or significantly altering the task. Although performance accuracy deteriorated significantly in the delayed feedback procedure in our study, a suitable proportion of correct trials (near 50%) was obtained and this allowed us to fully evaluate both the SPP and FRN. To examine appraisal processes one could adopt any motor task on which feedback is contingent. Thus, the compound of positivities seems to give rise to a procedural flaw in the SPT. The performance results in this experiment were inconsistent with previous studies in the area of motor control and learning that have reported deterioration in performance with the immediate or instantaneous feedback relative to the delayed-feedback presentation that provides participants with processing time inducing subjective-error estimation (Swinnen et al., 1990). This discrepancy might be due to dependency on external feedback in the SPT task rather than on intrinsic feedback that was essential in previous studies. On the other hand, previous studies also suggested that delayed feedback may not be beneficial (or even detrimental) for dynamic skilled movements or complex tasks compared to simple tasks (for a review, see Wulf and Shea, 2002). Although the SPT did not require any dynamic movement, it was so difficult to control that the delayed feedback did not benefit the timing performance. Another problematic point in previous SPP studies is the ambiguous definition of skilled performance. Almost all previous studies of SPP have adopted the SPT task. In other words, it is a necessary condition to use the SPT to obtain SPP. If so, the SPP may only be observed during a very specific testing paradigm employing one particular set of behavioral responses (i.e., an SPT that is performed with the left and the right thumbs). Thus, it remains unclear whether or not the SPP can represent more general motor skills than the timing task of the SPT. As an exception, Fontani et al. (2007) recorded the SPP during a more complicated karate skill (i.e., a karate ridge hand strike named Ura-Shuto-Uchi). They reported an SPP peaking about 1500 ms after the movement. This is a much longer latency than in previous reports. Because they did not provide participants with any feedback, it is doubtful that the late positivity is truly an SPP. If one were to take the perspective that the SPP is actually a P300 associated with the feedback, it cannot be expected to obtain an SPP during a more general motor skill unless feedback or KR is presented. A necessary condition to obtain the SPP appears to be the presence of concrete feedback rather than employing a timing task. 5. Conclusions In this study, we obtained the SPP in the SPT condition regardless of the type of control. On the other hand, only the P2 was observed in the control conditions and the DFB condition. The finding that the SPP was not observed immediately after the right-button press in the DFB condition did not support the online performance-monitoring account of the SPP. Importantly, the SPP and the feedback-elicited P300 shared similar latency, morphology, and topography, supporting that both ERPs are identical. The present results also suggested that the FRN elicited by negative feedback was indeed superimposed on the SPP on incorrect trials, resulting in the reduced SPP in the SPT condition, because both FRN and the reduction of the SPP were limited over frontocentral regions. Therefore, it is reasonable to conclude that the SPP actually represents a feedback-elicited ERP that is comprised of both FRN and P300 characteristics, one superimposed on the other, rather than some form of performance evaluation. Acknowledgments We would like to thank Eriko Tanaka and Toru Karouji for their help with the data collection. We also thank Dr. Rolf Verleger and an anonymous reviewer for their helpful comments on earlier versions of this manuscript. This study was supported by a Grant-in-Aid for Scientific Research (C) 24530925 from JSPS.

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