Exp Brain Res (2009) 197:311–319 DOI 10.1007/s00221-009-1916-0
RESEARCH ARTICLE
Preparation and inhibition of interceptive actions Welber Marinovic Æ Annaliese M. Plooy Æ James R. Tresilian
Received: 26 April 2009 / Accepted: 17 June 2009 / Published online: 30 June 2009 Ó Springer-Verlag 2009
Abstract Two experiments aimed to provide an estimate of the last moment at which visual information needs to be obtained in order for it to be used to initiate execution of an interceptive movement or to withhold execution of such a movement. In experiment 1, we sought to estimate the minimum time required to suppress the movement when the participants were first asked to intercept a moving target. In experiment 2, we sought to determine the minimum time required to initiate an interceptive movement when the participants were initially asked to keep stationary. Participants were trained to hit moving targets using movements of a pre-specified duration. This permitted an estimate of movement onset (MO) time. In both experiments the requirement to switch from one prepared course of action to the other was indicated by changing the colour of the moving target at times prior to the estimated MO. The results of the experiments showed that the decision to execute or suppress the interception must be made no less than about 200 ms before MO. Keywords Human Inhibition Interception Motor control Movement Preparation
W. Marinovic (&) A. M. Plooy Perception and Motor Systems Laboratory, School of Human Movement Studies, The University of Queensland, Blair Drive, St Lucia 4072, Brisbane, QLD, Australia e-mail:
[email protected] J. R. Tresilian Department of Psychology, University of Warwick, Warwick, UK
Introduction Interceptive actions like hitting and catching moving objects involve initiating movement at an appropriate moment in time so that the hand, bat or racquet reaches a location on the object’s path (the interception location) coincident with the object’s arrival. Although much research has been conducted to determine the basis for initiating and executing simple interceptions (for reviews see Lacquaniti et al. 1993; Merchant and Georgopoulos 2006; Tresilian 2005), very little is known about how people abort or withhold the production of an interception. There have been a few studies that examined the ability to withhold responses in coincidence anticipation tasks (Carlsen et al. 2008; McGarry et al. 2003; Slater-Hammel 1960), which resemble interceptive actions in some respects (for review see Tresilian 1995), but no experimental studies of people’s ability to withhold interceptions have been conducted. An ability to quickly abort execution can be advantageous in racquet sports like tennis or badminton where a player does not want to make contact with the ball or shuttle if it is going ‘out’. In these situations the player has a very limited period of time within which to determine that the ball is going out and to abort the process of interception. It has long been accepted that interceptive actions are initiated when a perceived variable reaches a threshold or criterion value (e.g. Lacquaniti and Maioli 1989; Tresilian 2005). Both behavioural (Lacquaniti et al. 1993; Smith et al. 2001) and neurophysiological (Merchant et al. 2004; Merchant and Georgopoulos 2006) evidence supports this proposal. There is some controversy concerning exactly what perceived variable is used for initiation (Caljouw et al. 2004), but it appears to be one that carries information about the moving target’s time-to-contact (TTC) with
123
312
the interception location (Lacquaniti et al. 1993; Merchant and Georgopoulos 2006; Smith et al. 2001; Tresilian 2005). All existing models agree, therefore, that the production of interceptive actions involves a motor command generation process that is prompted into generating commands by a trigger signal produced when the perceived variable reaches criterion (Zago et al. 2009) and so share the basic structure shown in Fig. 1a. There is some debate concerning the nature of the command generating process. Some have proposed that it is a kind of motor program that is capable of generating commands without sensory input (Tresilian 2005; Tyldesley and Whiting 1975); others propose that it is a kind of sensorimotor transformation that continuously converts sensory input into motor commands (Dessing et al. 2002; Peper et al. 1994). Although it is not clear which is correct (Zago et al. 2009), the two proposals both suppose that a triggering process produces an initiating signal when a perceived quantity reaches criterion. Figure 1b shows the temporal sequence of events that occurs when making an interception according to the basic model structure of Fig. 1a. Command generation is initiated by a trigger signal produced when perceived TTC
Fig. 1 a Functional block diagram of the program model of interception. b Sequence of events in the program model. When the TTC of the moving target reaches criterion (a stimulus event) some time is needed to process the information and start command generation (the visual processing and transmission time). c Sequence of events in a simple RT experiment: a warning stimulus is presented first, followed by the IS. The command generation that triggers the movement is issued once the IS has been detected (EMD electromechanical delay)
123
Exp Brain Res (2009) 197:311–319
(assumed to be the relevant variable) reaches a criterion value (TTCcrit). This temporal sequence may be fit into a very small period of time: in baseball, for example, the time between the pitcher’s release of the ball (moving target first visible) and the hit may be less than 500 ms and can be similar for a batsman in cricket or a tennis player returning serve (Regan 1992; Watts and Bahill 1990). Thus, if the interception that the player is prepared to make is to be withheld, the suppression process must work quickly. Although people’s ability to withhold or abort execution of prepared interceptions has not been explicitly studied, the ability to withhold manual responses in laboratory reaction time (RT) tasks has been studied extensively (De Jong et al. 1990; Logan and Cowan 1984; Logan et al. 1984; Logan and Irwin 2000; McGarry and Franks 1997; Mirabella et al. 2009; Mirabella et al. 2006). In the standard simple RT protocol the participant’s task is to make a response as soon as possible following presentation of an imperative stimulus (IS). This protocol can be modified to study the ability to withhold responding by embedding within a sequence of standard RT trials, a few trials in
Exp Brain Res (2009) 197:311–319
313
which a stimulus is presented to indicate that the response should not be executed (the stop signal, SS): participants are instructed not to respond to the IS if an SS is presented. Typically, the SS is presented after the IS during the RT interval (Fig. 1c shows the temporal sequence of events in a simple RT task). A major empirical issue investigated in RT tasks is to determine the last moment that the SS can be presented and for there still to be sufficient time to prevent the response being executed. The primary purpose of the experiments reported here is to address this same issue using an interceptive task. As in the RT protocol, a SS was used on some trials to indicate to participants that they were not to intercept the target, whereas on others no SS was presented and interception was to proceed normally. Comparison of Fig. 1b and c shows that there are certain basic similarities between the events that occur in an RT task and those that occur in an interceptive task. However, an important feature of RT tasks is that the stimulus events that an action is made in response to (the IS) is under experimental control. In an interceptive task, the action is made in response to TTC (or similar stimulus information) reaching a criterion and this is not something that is under experimental control. This presents a problem: how to control the timing of the SSs so that the last moment at which there is still sufficient time for the response to be withheld can be determined. This was done by adopting a protocol that we have used in previous studies of preparatory states in interception (Marinovic et al. 2008b; Tresilian and Plooy 2006): participants are trained prior to the experimental session to make interceptive movements that last a specific time (the movement time, MT). This allows an estimate to be made of when the movement will start (the time of movement onset, MO) since the MT is known as is the time when the target is at the interception location (see ‘‘Materials and methods’’). The SS can then be presented at
different times prior to the estimated MO time, permitting an investigation of the latest time at which the SS can be presented and the interceptive response withheld. The results of the experiments presented in this report provide estimates for the time delays involved in the processes of inhibition and preparation of rapid interceptive actions.
Fig. 2 Plan view of the experimental setup of the interceptive task. The bat starts a distance of 28 cm from the target’s path. Point P is the point at which the centre of the bat meets the path of the target face. Point Q is at the centre of the target face. The grey shaded area is the
region swept out by the bat as it is moved along its track. The time to arrival of Q at P (the TTC) is Z(t)/V, where Z(t) is the distance of Q from P at time t
Materials and methods Subjects Ten volunteers participated in the experiments and all gave their informed consent prior to commencement of the study, which was approved by the local Ethics Committee of the University of Queensland. All participants reported normal or corrected to normal vision and stated they were right handed. Their ages ranged from 25 to 38 years. Apparatus and task The experimental task was to hit a moving target performing a movement of 180 ms of duration. The target was mounted on a carriage, which was attached to a belt system driven by computer controlled torque motor. The participants were constrained to move a bat along a straight path above and perpendicular to the target track as shown in Fig. 2. The target was made of slightly abraded clear plastic material with embedded LEDs which illuminated the target with either a green or red colour. The target was flat and rectangular (9 cm tall and 6.1 cm in length) and it was seen for 2.2 s before its arrival at the strike zone in all trials (grey shaded area in Fig. 2), and it moved with a constant velocity of 1.5 m/s. Ambient light was dim, so that the target was distinctive, but it did not impair vision of the
123
314
surrounding objects. Details of the experimental setup can be found elsewhere (Marinovic et al. 2008). Infrared emitting diodes (IREDs) were fixed to the bat and to the carriage in which the target was housed. The positions of these IREDs were sampled at 200 Hz during experimental trials using an Optotrak (Northern Digital Inc.) optoelectronic movement recording system and stored on computer disc. Surface EMG data were collected using bipolar preamplified electrodes with an analogue bandpass filter (30– 500 Hz) built into the preamplifiers. The two electrodes were circular (diameter 4 mm) mounted 9 mm apart in an insulating block (23 9 15 9 3 mm) which housed the preamplifier. The preamplifier gain was adjustable from 24 to 2,200. Surface EMG activity was recorded from the bellies of the right anterior deltoid (AD) and right posterior deltoid (PD). A grounding electrode was placed on the right acromion. During experimental trials EMG data were sampled at 1,000 Hz by the OptotrakTM analogue-to-digital data acquisition unit (ODAU unit, Northern Digital Inc.) and recording was time-locked to the recording of the IRED position data.
Design and procedures Experiment 1 Prior to the experimental session, the participants were trained to hit the target with a movement time of 180 ms so that movement onset time could be estimated in advance. During training and experimental sessions the participants were provided with knowledge of results (KR) about their performance. The KR informed the participants about their MTs and maximum distance moved. In experiment 1 participants’ primary task was to intercept the target with the specified MT. The target was always initially illuminated by the green (go signal) LED throughout its trajectory towards the interception location. However, on 50% of the trials (nogo trials), when the target colour changed from green to red (stop signal), they were required to halt their movements. The stop signal was presented pseudorandomly. The stop signal (colour change) on nogo trials could occur at various times prior to the expected moment of movement onset (i.e. 180 ms prior to the target reaching the hitting location). Five different stop signal intervals were used: 50 (SS-50), 100 (SS-100), 150 (SS-150), 200 (SS-200), and 250 ms (SS-250). To balance order effects of task presentation, half of the participants began the experimental session with experiment 1, and half of them began with experiment 2. The participants performed eight trials for each of the five conditions in which there was a
123
Exp Brain Res (2009) 197:311–319
colour change plus 40 control trials (no colour change) in each of the two experiments (160 total). Experiment 2 The participants’ primary task was to keep the bat stationary. The target was initially illuminated by the red (nogo signal) LED throughout its trajectory towards the interception location. However, on 50% of the trials (go trials), when the target colour changed from red to green (go signal), they were required to strike the target with the specified MT of 180 ms. The go signal was presented pseudorandomly. The go signal on go trials could occur at various times prior to the expected moment of movement onset. Five different preparation intervals were used: 100 (PI-100), 150 (PI-150), 200 (PI-200), 250 (PI-250) and 500 ms (PI-500).
Data reduction and analysis Experiment 1 Data reduction was performed using custom Labview software (version 7.1, National Instruments). The position data time series were digitally filtered by dual pass through a second order Butterworth filter with a cut-off frequency of 20 Hz. Movement onsets were estimated from the tangential velocity time series (derived by numerical differentiation from the filtered position time series) using the two-stage algorithm recommended by Teasdale et al. (1993). When an interception was required, the time at which the target was hit as well as the temporal error (TE) were estimated from the position time series of the bat IRED and the target IRED. Further details of the analysis procedures can be found elsewhere (Marinovic et al. 2008). The EMG data obtained from each muscle were fullwave rectified, and digitally enveloped by dual-pass through a low-pass, second order Butterworth filter with a 51-Hz cutoff (equivalent to fourth order, zero phase lag filter with a 40-Hz cutoff). The main measure in experiment 1 was the absence or presence of movement. A failure to withhold a movement was considered as such if the participant moved the bat more than 10 mm and the EMG showed an activation of the AD which exceeded three standard deviations from baseline activity for more than 20 samples. To obtain inhibition functions, the data set of each participant was fitted with a cumulative Gaussian by using a maximumlikelihood fitting procedure. The time required to suppress the interceptive action was defined as the point in the inhibition function at which the probability of inhibiting the movement was 0.5. In this experiment, we also
Exp Brain Res (2009) 197:311–319
315
analysed: Amax, defined as the highest value in the acceleration profile. Distance moved, defined as the maximum distance the bat moved away from its initial position. EMG amplitude defined as the peak of enveloped EMG activity. Effects of experimental conditions on Amax, distance moved, and EMG amplitude were first analysed through a one-way ANOVA with repeated measures. A Newmann– Keuls post hoc test, P \ 0.05, was used for comparison of the means. Experiment 2 The variables of interest were MT, defined as the time between movement onset and target strike. Peak acceleration (Amax), defined as in experiment 1. TE, defined as the difference between target strike time and the time the centre of the target reaches the interception location. If the bat arrived before the centre of the target at the interception location, the temporal error was early and recorded as negative, otherwise the error was positive. For each participant the mean of the eight trials in each experimental condition was averaged to give estimates of MT, Amax, and constant TE (CTE) for each condition (both hits and misses were used in the calculation of these variables). The procedures and design for the analyses of these variables were the same as those used in experiment 1.
Results Experiment 1 In Fig. 3 is shown the inhibition function for two representative participants. As shown in Fig. 3, the probability of inhibiting a prepared hitting action was virtually zero up to 100 ms before movement onset, but rapidly increased after this point. In fact, for all participants only one response was completely inhibited when the stop signal interval was \150 ms. Since we controlled the timing of the stop signal appearance based on the estimated movement onset time, the mean stop signal time required to withhold the hitting action should be equal to the point at which the inhibition function reaches 0.5. The mean (±SD) stop signal interval estimated with this approach across all of the subjects was 192 ms (±26.3). As shown in Fig. 4a, on average the participants reached the target’s plane of motion (280 mm from the starting position) only when the time left to withhold the action was in the order of 50 ms. A repeated measures ANOVA on this variable revealed a significant effect of stop signal interval, F(5, 40) = 138.52, P \ 0.0001, x2 = 0.87. Post
Fig. 3 Inhibition functions for two representative subjects (P8 and P9). The curves are the cumulative Gaussian functions that best fit the data. The grey lines in each panel indicate the point in the inhibition function at which the probability of inhibiting the movement was 0.5. Filled circles represent the proportion of inhibited trials at that particular SS interval
hoc analysis showed that the distance moved was greater for each decrement in the stop signal interval since all pairwise comparisons were significant. Figure 4b shows that Amax decreased gradually as the stop signal interval became longer. A repeated measures ANOVA on this variable revealed a significant effect of stop signal interval, F(5, 40) = 97.03, P \ 0.0001, x2 = 0.86. Post hoc analysis showed that Amax was significantly different for all pairwise comparisons, except for those between the SS interval of 250 and 200 ms, and between the SS interval of 50 ms and go-trials in which Amax did not differ from each other. Repeated measures ANOVAs on the peak amplitude of enveloped EMG revealed that significant differences existed in AD, F(5, 40) = 23.86, P \ 0.0001, x2 = 0.62, and PD, F(5, 40) = 5.78, P \ 0.0001, x2 = 0.22. Pos hoc analysis on AD showed that peak amplitude was lower than on go trials only at SS intervals of 150, 200, and 250 ms as shown in Fig. 4c. By contrast, the post hoc analysis on PD indicated that peak amplitude was larger than in go trials at SS intervals of 50, 100 and 150, but not at 200 and 250 ms as shown in Fig. 4d. Experiment 2 Figure 5 shows MT, CTE, and Amax data from experiment 2. In Fig. 5a, the dashed line indicates the required MT with which the moving targets should be intercepted, whereas the dotted lines indicate the range within which MT was considered acceptable. As can be seen in Fig. 5a, MT decreased gradually as the preparation interval became shorter and when the preparation interval was equal or shorter than 150 ms the participants could not produce
123
316
Exp Brain Res (2009) 197:311–319
Fig. 4 a Mean distance moved on nogo and go trials as a function of SS interval. Dashed line indicates the distance between the initial position and the plane of target movement, where the target could be hit. b Mean maximum acceleration on nogo and go trials as a function of SS interval. c–d Mean peak amplitude expressed as a proportion of mean go trial amplitude for each muscle as a function SS interval. c Anterior deltoid (AD). d Posterior deltoid (PD). The error bars show 95% confidence intervals
MTs with the specified duration (180 ms ± 10%). The repeated measures ANOVA on MT revealed a significant effect of preparation interval, F(4, 36) = 27.66, P \ 0.0001, x2 = 0.52. Post hoc analysis confirmed that MT was greater for each increment in the preparation interval with all pairwise comparisons being significant, except for those between PI-100 and PI-150 in which MTs did no differ from each other. Figure 5b shows that the participants tended to arrive at the interception zone late when the preparation interval was in the order of 150 ms or less. In contrast, with preparation intervals of 200 ms or greater, there was a tendency to arrive at the interception zone earlier. The repeated measures ANOVA on CTE indicated a significant effect of preparation interval, F(4, 36) = 94.34, P \ 0.0001, x2 = 0.88. Post hoc analysis showed that CTE in conditions PI-100 and PI-150 differed from all other conditions, whereas pairwise comparisons among conditions PI-200, PI-250 and PI-500 showed no differences. Figure 5c shows that Amax decreased gradually as the preparation interval became longer. The repeated measures ANOVA on Amax revealed a significant effect of preparation interval, F(4, 36) = 9.48, P \ 0.0001, x2 = 0.40. Post hoc analysis showed that Amax in conditions PI-100 and PI-150 was greater than those observed in conditions PI-200, PI-250, and PI-500, but they did not differ from each other.
participants delaying the time of MO to increase the time available for inhibition). For this purpose we compared go trials in experiment 1 with conditions in which the participants had enough time to prepare their responses (PI-250 and PI-500). The variables compared were: MT, CTE and Amax. A repeated measures ANOVA comparing MT on go trials of experiment 1 and MT at long preparations intervals in experiment 2 showed a significant effect of condition, F(2, 18) = 6.32, P \ 0.01, x2 = 0.18. The post-hoc test showed that MT at PI-500 ð x ¼ 190:1 msÞ in experiment 2 was longer than that observed at PI-250 ð x ¼ 177:6 msÞ in experiment 2 and also longer that observed in go trials of experiment 1 ð x ¼ 177:8 msÞ; which did not differ from each other. This indicates that the participants produced accurately the required MT of 180 ms (±10%) on go trials in experiment 1 since performance on this condition did not differ from that on PI-250 in experiment 2, when the participants had a better performance in producing the required MT than on PI-500 (see Fig. 5a). Furthermore, the repeated measures ANOVAs revealed neither a significant effect on CTE, F(2, 18) = 3.34, P [ 0.05, x2 = 0.10, or Amax, F(2, 18) = 0.99, P [ 0.05, x2 = 0.01. These results suggest that the participants were preparing to strike the moving target, as trained, without being affected by the high probability of inhibiting their movements on nogo trials.
Comparison between experiments 1 and 2
Discussion
We also conducted additional comparisons between the two experiments. These comparisons are important because the expectation of a SS in experiment 1 could affect the time course of preparation for the interception (e.g.
In the experiments reported here we investigated the time course of inhibitory and preparatory processes of fast interceptive actions. Whereas some experiments have studied the time course of movement preparation of
123
Exp Brain Res (2009) 197:311–319
Fig. 5 a Mean movement time on go trial conditions. Dashed line indicates the required MT. Dotted lines indicate the range within which MT was considered to be correct (±10%). b Mean constant temporal error in go-trial conditions. c Mean maximum acceleration in go trial conditions. The error bars show 95% confidence intervals
interceptions during the 0.5 s prior to movement onset (Marinovic et al. 2008b), to our knowledge no experiment to date has investigated peoples’ ability to inhibit this type of action. A number of experiments investigating movement suppression in RT tasks have used the ‘‘race model’’ put forward by Logan and Cowan (1984) and Logan et al. (1984) as a tool to investigate the dynamics of inhibitory processes (De Jong et al. 1990; Logan and Cowan 1984; Logan et al. 1984; Logan and Irwin 2000; McGarry and Franks 1997; Mirabella et al. 2009; Mirabella et al. 2006). In their model, Logan and colleagues proposed that activation and inhibition evolve independently of one another and compete for control of responding. If the excitatory process is completed first, a response is produced. If the inhibitory process is completed first, a response does not occur. This description of the competition between internal processes involved in the production and inhibition of RT
317
tasks is somewhat analogous to the triggering and inhibition processes involved in interceptions. The commandgenerating process activated by the perceived variable (TTCcrit in Fig. 1b) reaching criterion in an interception is analogous to the activation of excitatory processes activated by an IS in a RT task. Also, the inhibitory processes in RT tasks and interceptions are both initiated when an external stop signal is presented (although in RT tasks the stop signal is presented after the IS, whereas in interceptions it can only be presented in relation to when the response is expected to occur). Therefore, despite the obvious differences in the protocols used to study inhibition in RT tasks and interceptions, it seems that the race model proposed by Logan and colleagues is, at least qualitatively, equivalent to the competition between the triggering and inhibition processes we believe are involved in the suppression of rapid interceptive actions. This seems to indicate that the MT training protocol used to make our participants initiate their movements at a particular moment may be an alternative to study inhibitory processes in more complex motor acts (e.g. intercepting moving objects) in a similar manner that the race model allows the study of inhibition in RT tasks. In experiment 1, we sought to determine the minimum time needed to suppress fast interceptive actions. In this experiment, MT on go trials was produced accurately by the participants and CTE and Amax were similar to the values observed in experiment 2 for long preparation intervals (C250 ms). This suggests that the participants were not affected by the expectation of suppressing their movements and prepared their actions as requested. As a result, movement onset time can be estimated in advance of the person starting to move and so the amount of time available to inhibit this type of action can be controlled. The results of experiment 1 showed an average time in the order of 192 ms to inhibit a hitting action. This latency is close to that reported for other manual responses (Logan et al. 1984; Logan and Irwin 2000; Mirabella et al. 2009; Mirabella et al. 2006), but greater than the values found for the suppression of other anticipatory tasks, which seems to be about 150 ms (Carlsen et al. 2008; McGarry et al. 2003; Slater-Hammel 1960). One possible account for the discrepancy between the results obtained with other anticipatory tasks and the results here presented is based on the requirements imposed by the different tasks. The participants in experiment 1 were asked to produce movements of a specified duration to intercept a moving target. In previous studies with anticipatory tasks (Carlsen et al. 2008; McGarry et al. 2003; Slater-Hammel 1960) there was no MT requirement and movement onset had simply to coincide with the arrival of the target at a specific location. Since our participants had to move for approximately 180 ms after
123
318
movement onset, the critical moment for temporal estimation of the target’s arrival at the contact point was made well before that of previous studies with anticipatory tasks. Gray and Regan (1998) found that the variance in TTC estimation can be expressed as a percentage of TTC. Consequently, the determination of movement onset time might have been temporally less precise in our task because of longer estimations of TTC values in which the movement should be triggered. This may have required our participants to program and store their responses in advance (in case they overestimated the real TTC value and had to initiate their responses sooner than expected). In addition, whereas in previous experiments (Carlsen et al. 2008; McGarry et al. 2003; Slater-Hammel 1960) the success in a trial depended mainly on movement onset timing, in our task movement onset was an initial component of the task since the movement should be programmed to bring the limb to a determined place with a specific duration. Therefore, motor preparation well in advance of movement initiation was likely to be more important in our task than in previous experiments with anticipatory tasks (Carlsen et al. 2008; McGarry et al. 2003; Slater-Hammel 1960). As a result, it may have been more difficult to inhibit an action in our experiment because the preparatory processes were in more advanced stages than in other anticipatory tasks previously studied. An alternative account for the additional delay to inhibit an interceptive action in our experiment may reside on the utilisation of colour change to indicate that the response should be halted.1 Pisella et al. (1998) showed that the latency to stop an ongoing reaching action in response to a colour change is longer than that observed to stop in response to a location change (however, see Brenner and Smeets 2004). Previous research investigating inhibition in anticipatory tasks used either an acoustic stimulus (Carlsen et al. 2008) or the sudden stop of the moving target which indicates the time of movement onset (McGarry et al. 2003; Slater-Hammel 1960). Therefore, an alternative hypothesis is that the additional delay we obtained was due to a slower processing rate for colour change in comparison to acoustic and location stimuli. Note that the two hypotheses we have raised here, advanced preparation and colour change, are not mutually exclusive and thus it is possible that both may have played a role in determining the latency to inhibit movements in our experiment. Further experiments are warranted to distinguish between these two alternative hypotheses. The results of experiment 1 also showed that although virtually no response could be completely withheld when the stop signal was presented 100 ms before movement onset, the response produced was affected. When the stop 1
We thank one anonymous reviewer for raising this possibility.
123
Exp Brain Res (2009) 197:311–319
signal was delivered 100 ms before movement onset, the value of peak acceleration (Amax) was significantly reduced. Analysis of peak EMG amplitude indicated that the prepared responses were affected by the stop signal. However, rather than a reduction in the activation of agonist muscles (AD) at SS intervals B100 ms, there was a significant increase in the activation of antagonist muscles (PD). This result indicates that the stop process could not affect the initial phase of the prepared response when delivered 100 ms before movement initiation, but suggests that the activation of antagonist muscles could be rapidly increased to stop the ongoing action. When the stop signal was presented 50 ms before movement onset, however, there was no time to increase the activation of antagonist muscles and consequently most responses reached the interception zone. In fact, many responses on nogo trials at the stop signal interval of 50 ms were carried out to completion and 56% (±19.7) of them hit the target. These findings suggest that about 50 ms before movement onset it was too late to initiate any amendment to the movement that could be effectively used during a rapid interceptive action. The results, therefore, are consistent with a motor program model for the control of brief interceptive actions where visual information can only play a minor role after movement initiation. Note that the increased activation of antagonist muscles after movement onset refers to a process of movement suppression which is different from the race between inhibitory and triggering processes described in the introduction since the race had already been won by the triggering process. In this case, the SS may have been responsible for initiating a counteracting response intended to stop an ongoing action as soon as possible. This counteracting response, however, seemed to be only triggered when there was an overt action since there was no indication of increased antagonist, nor agonist, muscle activity on successfully inhibited trials. In experiment 2, we manipulated the preparation interval of a hitting action by presenting on 50% of the trials a go signal which was delivered at different moments before the expected movement onset time. The results showed that under uncertain knowledge about the requirement to move or not, participants could produce hitting actions accurately, in terms of movement time and the temporal error to hit the target’s centre, with a preparation interval as short as 200 ms. This latency is similar to that we found for the preparation of an interceptive action in a previous study where the participants had to prepare for one out of two distinct movement amplitudes in a trial-by-trials basis (Marinovic et al. 2008). The comparison between participants’ performance with preparation intervals C200 ms in experiment 2 and that observed in experiment 1 in go trials (no SS presented) suggests that the expectation to withhold the action did not affect the time course of motor
Exp Brain Res (2009) 197:311–319
preparation in experiment 1. Assuming that participants’ performance would deteriorate if the go-signal was delivered after TTC information had reached the criterion value of the initiating variable, experiment 2 also provides an estimate of the interval in which TTC reaches criterion. Since performance was negatively affected when the gosignal was presented after 150 ms to movement onset, we conclude that the triggering variable was produced between 150 and 200 ms prior to movement onset. This result is consistent with the triggering signal occurring about 150 ms prior to movement onset as we have recently shown (Marinovic et al. 2009; Tresilian and Plooy 2006). In summary, the results of the experiments reported showed that the decision to perform or inhibit a rapid interception must be made no less than about 200 ms before movement onset. Although both preparatory and inhibitory processes span similar durations, an advantage of the inhibitory process is that if a visual cue to withhold the movement is delivered, for example, about 100 ms before movement onset, the performer might be able to prevent the completion of an already initiated action. In contrast, the preparatory process cannot be shorter than about 200 ms before movement onset without a sacrifice in performance levels. Acknowledgments This research was supported in part by a CAPES (Postgraduate Federal Agency/Brazilian Government) doctoral scholarship to Welber Marinovic and a grant from the Australian Research Council awarded to J. R. Tresilian and A. Plooy.
References Brenner E, Smeets JBJ (2004) Colour vision can contribute to fast corrections of arm movements. Exp Brain Res 158:302–307 Caljouw SR, van der Kamp J, Savelsbergh GJP (2004) The fallacious assumption of time-to-contact perception in the regulation of catching and hitting. In: Hecht H, Savelsbergh GJP (eds) Timeto-contact. Elsevier Science, Amsterdam, pp 443–474 Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2008) Motor preparation in an anticipation-timing task. Exp Brain Res 190:453–461 De Jong R, Coles MGH, Logan GD, Gratton G (1990) In search of the point of no return—the control of response processes. J Exp Psychol Hum Percept Perform 16:164–182 Dessing JC, Bullock D, Peper CE, Beek PJ (2002) Prospective control of manual interceptive actions: comparative simulations of extant and new model constructs. Neural Netw 15:163–179 Gray R, Regan D (1998) Accuracy of estimating time to collision using binocular and monocular information. Vision Res 38:499– 512 Lacquaniti F, Maioli C (1989) The role of preparation in tuning anticipatory and reflex responses during catching. J Neurosci 9:134–138 Lacquaniti F, Corrozzo M, Borghese NA (1993) The role of vision in tuning the anticipatory motor responses of the limbs. In: Berthoz A (ed) Multisensory control of movement. Oxford UP, Oxford, pp 379–393
319 Logan GD, Cowan WB (1984) On the ability to inhibit thought and action—a theory of an act of control. Psychol Rev 91:295–327 Logan GD, Irwin DE (2000) Don’t look! Don’t touch! Inhibitory control of eye and hand movements. Psychon Bull Rev 7:107– 112 Logan GD, Cowan WB, Davis KA (1984) On the ability to inhibit simple and choice reaction-time responses—a model and a method. J Exp Psychol Hum Percept Perform 10:276–291 Marinovic W, Plooy AM, Tresilian JR (2008a) The time course of amplitude specification in brief interceptive actions. Exp Brain Res 188:275–288 Marinovic W, Plooy AM, Tresilian JR (2008b) The time course of direction specification in brief interceptive actions. Exp Psychol (in press) Marinovic W, Plooy AM, Tresilian JR (2009) The utilisation of visual information in the control of rapid interceptive actions. Exp Psychol 56:265–273 McGarry T, Franks IM (1997) A horse race between independent processes evidence for a phantom point of no return in preparation of a speeded motor response. J Exp Psychol Hum Percept Perform 23:1533–1542 McGarry T, Chua R, Franks IM (2003) Stopping and restarting an unfolding action at various times. Q J Exp Psychol A 56:601– 620 Merchant H, Georgopoulos AP (2006) Neurophysiology of perceptual and motor aspects of interception. J Neurophysiol 95:1–13 Merchant H, Battaglia-Mayer A, Georgopoulos AP (2004) Neural responses during interception of real and apparent circularly moving stimuli in motor cortex and area 7a. Cereb Cortex 14:314–331 Mirabella G, Pani P, Pare´ M, Ferraina S (2006) Inhibitory control of reaching movements in humans. Exp Brain Res 174:240–255 Mirabella G, Pani P, Ferraina S (2009) The presence of visual gap affects the duration of stopping process. Exp Brain Res 192:199– 209 Peper L, Bootsma RJ, Mestre DR, Bakker FC (1994) Catching balls: how to get the hand to the right place at the right time. J Exp Psychol Hum Percept Perform 20:591–612 Pisella L, Arzi M, Rossetti Y (1998) The timing of color and location processing in the motor context. Exp Brain Res 121:270–276 Regan D (1992) Visual judgments and misjudgements in cricket, and the art of flight. Perception 21:91–115 Slater-Hammel AT (1960) Reliability, accuracy, and refractoriness of a transit reaction. Res Q 31:217–228 Smith MRH, Flach JM, Dittman S, Stanard T (2001) Monocular optical constraints on collision control. J Exp Psychol Hum Percept Perform 27:395–410 Teasdale N, Bard C, Fleury M, Young DE, Proteau L (1993) Determining movement onsets from temporal series. J Mot Behav 25:97–106 Tresilian JR (1995) Perceptual and cognitive processes in time-tocontact estimation: analysis of prediction-motion and relative judgment tasks. Percept Psychophys 57:231–245 Tresilian JR (2005) Hitting a moving target: perception and action in the timing of rapid interceptions. Percept Psychophys 67:129– 149 Tresilian JR, Plooy AM (2006) Effects of acoustic startle stimuli on interceptive action. Neuroscience 142:579–594 Tyldesley DA, Whiting HTA (1975) Operational timing. J Hum Mov Stud 1:172–177 Watts RG, Bahill AT (1990) Keep your eye on the ball: the science and folklore of baseball. Freeman, New York Zago M, McIntyre J, Senot P, Lacquaniti F (2009) Visuo-motor coordination and internal models for object interception. Exp Brain Res 192:571–604
123
