Exp Brain Res (2004) 156: 518–523 DOI 10.1007/s00221-004-1911-4

RESEARCH NOTES

Sukhvinder S. Obhi . Patrick Haggard

Internally generated and externally triggered actions are physically distinct and independently controlled

Received: 7 November 2003 / Accepted: 22 March 2004 / Published online: 15 May 2004 # Springer-Verlag 2004

Abstract In everyday life we must constantly balance our intentions to act in a certain way with reactions that are imposed upon us by the outside world. Recent neuroimaging studies have examined these classes of movement separately but despite the fundamental requirement for us to efficiently organize our internally generated and externally triggered actions, few studies have examined the relationship between these two classes of movement. We measured EMG activity in the right first dorsal interosseous while subjects performed right index finger key presses either in an internally generated condition or an externally triggered condition. In addition, in an attempt to probe the relationship between the processing underlying these two types of action, we examined the effect on reaction time (RT) and EMG activity in a third “truncation” condition in which subjects were forced to switch from an intentional (internally generated) mode of response production to an externally triggered mode. Results indicated significantly greater muscle activation for actions that were internally generated as compared to externally triggered. Truncation caused responses to be delayed by, on average, 54.7 ms as compared with simple externally triggered responses, suggesting that the motor system cannot take advantage of preexisting levels of preparation when switching between internally generated and externally triggered actions. Interestingly, the unique EMG signatures of internally generated and externally triggered actions were preserved in truncation. Thus, subjects switched between the two types of action rather than simply modifying an ongoing action. The results provide peripheral physiological support for previous S. S. Obhi (*) CIHR Group on Action & Perception, Room 6246, Department of Psychology, University of Western Ontario, London, Ontario, N6A 5C2, Canada e-mail: [email protected] S. S. Obhi . P. Haggard Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London, WC1 N 3AR, UK

neuroimaging work suggesting that internally generated actions are preceded by greater levels of preparation than externally triggered actions. The present findings also raise the interesting possibility that the motor system processes these two classes of action separately even though the motor output required is the same. Keywords EMG . Externally triggered actions . Internally generated actions . Motor system . Movement preparation

Introduction In everyday life, in order to function successfully, we constantly have to balance reactions to external stimuli with our internally generated actions. A striking example of what happens when this balance is lost comes from individuals who exhibit utilization behavior (UB). This disorder is often the result of bilateral damage to the medial parts of the frontal lobe, especially the supplementary motor area (SMA) (Boccardi et al. 2002). Individuals with UB cannot help but respond to and interact with objects they come across in the environment around them, even if such responses are inappropriate. One possible account of such cases is that the lateral parts of the premotor cortex (PMC) dominate motor planning when the more medial SMA is damaged. The lateral PMC has been previously shown in non-human primates to direct movement on the basis of external cues, whereas the SMA has been suggested to direct movements on the basis of internal processes (e.g., Passingham et al. 1987; Halsband et al. 1994). Despite the fundamental requirement for a functional balance between reactions to external stimuli and internally generated actions, most studies have examined each of these types of action separately. That is, surprisingly little research has focused on the interaction between these two classes of action. The aim of this experiment was to redress this imbalance in the literature. In contrast to non-human primates, the evidence for the existence of two functionally specialized premotor systems in humans is less convincing. It has been shown that

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several brain areas are involved in the production of both internally generated actions and externally triggered actions (Jahanshahi et al. 1995). These areas include the dorsolateral prefrontal cortex (DLPFC), SMA, anterior cingulate, the lateral PMC, parietal area 40, insular cortex, the thalamus and the putamen. In addition the peak component of the bereitschaftspotential (a movementrelated cortical potential that reflects motor preparation and is measured over medial frontal motor structures including the SMA) was greater in self-initiated movements compared with externally triggered movements. Other studies have also found a similar network of brain areas to be active in both classes of action but a greater (or more sustained) activation in medial frontal areas for internally generated actions compared with externally triggered actions (e.g., Jenkins et al. 2000; Cunnington et al. 2002). These findings are consistent with the notion that the SMA is somewhat more involved in preparation for self-initiated actions than externally triggered actions, and is thought to be the generator of the early component of the bereitschaftspotential (Deecke 1990). Although generally considered as an index for voluntary, selfinitiated movement, the bereitschaftspotential has been observed in predictably cued externally triggered actions, albeit with reduced amplitude (e.g., Jahanshahi et al. 1995). One way to investigate the independence or otherwise of these systems is to measure whether and how they might interact. Consider an individual preparing to make an internally generated key press who is suddenly cued via an external stimulus to make the same key press. What would happen to the reaction time (RT) of the key press as compared to a situation in which the individual was externally cued whilst not preparing to make an internally generated key press? One possibility is that, if the motor system can take advantage of the existing levels of motor preparation, responses to external stimuli should be facilitated as compared to when responses are made to the same external stimuli in the absence of internal preparation to make the same action. However, recent work by Astor-Jack and Haggard (2004) has investigated this question and found the opposite result. These authors described a “truncation” task, in which preparation for a voluntary (internally generated) action was truncated, or interrupted by an external stimulus requiring the same motor response that the subject was already preparing. RT was delayed as compared to a condition in which subjects simply responded to an auditory stimulus when not preparing internally generated actions. This result suggests that internally generated and externally triggered actions are incompatible even when the motor output required is the same. This RT cost of internal preparation was found to be robust in several experiments and is not due to changes in the processing of the stimulus, since stimulus-locked evoked potentials were not delayed or attenuated. Those authors emphasized that the subject performed the same action, typically a button press, in both internally generated and externally triggered conditions. While these movements were indeed behaviorally similar, the authors

did not report the physical parameters of the movement in detail. Other studies of internally generated and externally triggered actions have similarly assumed that these actions are physically comparable (e.g., Cunnington et al. 2002). This issue is psychologically interesting for two reasons. First, any significant physical differences between the two classes of action would support the view that they are controlled by separate brain circuits. Second, the physical form of movements in the truncation condition may show whether subjects can integrate the characteristic movement patterns of internally generated and externally triggered actions to create a “hybrid” movement, or whether they switch discretely between the two patterns. This issue would clarify the relations between these two classes of action.

Methods Subjects Twelve right-handed subjects aged 25.8±3.4 years took part in the experiment, which was approved by the local ethics committee. Subjects gave their written consent, and local ethical guidelines were followed. Subjects sat at a desk in a quiet room, with their right index finger resting on the end of a lever. Each subject performed five practice and 28 “real” experimental trials in each of three conditions. The order of conditions was counterbalanced across subjects.

Apparatus Subjects made both intentional and reactive movements by flexing their right index finger on a metal lever. EMG of the first dorsal interosseus muscle of the right hand was measured with surface electrodes. The stimuli for reactive movements were taps delivered to the back of the subject’s neck in the midline by an unseen experimenter. Tactile stimulation was recorded by a force sensor positioned on the subject’s neck at the point of contact of the tap. EMG and tactile stimulation traces were recorded on a computer for off-line analysis.

Task details The three experimental conditions comprised an internally generated movement condition, an externally triggered movement condition and a truncation condition. In the externally triggered movement condition, a simple RT paradigm was employed. After the experimenter had warned the subject of the start of the trial using a “trial starts” instruction, a tactile stimulus in the form of a finger tap to the back of the neck was delivered. The intensity of the imperative stimulus was registered via a force sensitive resistor that was attached to the back of the subject’s neck. The stimulus was delivered in such a way that subjects had no prior information about when they would be required to respond (i.e., the experimenter was out of view during experimental trials). The interval between the experimenter’s verbal warning and delivery of the tactile stimulus, i.e., fore-period, varied randomly between 3–10 s. Subjects were instructed to respond with a right index finger press as fast as possible upon sensing the stimulus. The subject’s finger press ended the trial and after a short inter-trial interval the experimenter indicated the beginning of the next trial. In the internally generated movement condition, subjects were instructed to make the same right index finger press at a time of their

520 own choosing. The only constraint was that they had to try and randomly vary their movement such that it occurred within a 3–10 s range. This is the same time range that the imperative stimulus was delivered within in the externally triggered movement condition. In the internally generated condition there was no external imperative stimulus of any kind. Lastly, in the truncation condition subjects were asked to initiate and prepare an internally generated voluntary press with the right index finger at a time of their own choosing. Subjects were particularly instructed not to act in a stereotyped or rhythmic manner. A tactile stimulus was delivered at a random time during the trial, as in the externally triggered condition. Subjects were instructed to respond to the tactile stimulus as fast as possible with a right index finger press. Thus, subjects could make either an internally generated or an externally triggered press, according to whether or not the stimulus occurred before their internal process of preparation had produced the movement. In either case a press with the right index finger signified the end of trial. In the truncation condition, to ensure that it was possible to interrupt the internal preparation with a tactile stimulus, subjects were instructed to “make their responses randomly within about 3– 10 s after the onset of the trial”. This 3–10 s range corresponds to the range of times from which the delivery times of the tactile stimulus were sampled. Thus, on some trials subjects made their internally generated response prior to delivery of the tactile stimulus. These trials were termed intentional truncation trials. On most other trials, the tactile stimulus was delivered prior to subjects making their internally generated response and subjects reacted to this stimulus. These trials were termed reactive truncation trials. In this way the truncation condition resulted in two sets of trials (internally generated and reactive truncation). These subdivisions of the truncation condition were treated as two conditions for purposes of analysis. On a small number of remaining trials, subjects made the response very soon after delivery of the tactile stimulus. As we were measuring RTs with respect to EMG onset, any response made in less than 75 ms after the stimulus was excluded from the analysis, since it could not be conclusively classified as intentional or reactive. To test for the effects of truncation, reactive truncation trials were compared to trials in the externally triggered movement condition and intentional truncation trials were compared to trials from the internally generated movement condition.

Data analysis After first rectifying the EMG data, the onset and offset of the main EMG burst were selected interactively and the waveform was integrated between these limits to represent the total muscle activity associated with the action. The mean of this measure for each subject in each condition was calculated and statistics were performed on these values. The time of tactile stimulation in reactive trials was determined interactively by inspecting the force sensor trace and marking the onset of applied force. The interval between stimulus onset and EMG burst onset was used as a measure of RT. Any RTs greater than 1,000 ms were classed as missed trials and were not analyzed.

Fig. 1 Median trials showing raw EMG in internally generated and externally triggered conditions. Dashed line indicates time of stimulus presentation

Main effects of type of movement Figure 2 shows the rectified EMG activity in the first dorsal interosseous for internally generated and externally triggered movements. A repeated measures ANOVA confirmed that there was a main effect of type of movement on rectified EMG activity with internally generated movements generating significantly greater EMG activity than externally triggered movements (F(1,10)=5.210, p=.046). In addition, the duration of EMG activity in internally generated actions was longer than the duration of EMG activity in externally triggered actions but this difference just failed to reach statistical significance (F(1,10)=3.861, p=.078). Main effects of truncation There were no significant main effects of truncation on EMG activity (F(1,10)=1.088, p=.322) or duration of EMG activity (F(1,10)=1.365, p=.270). Interactions between the type of movement and truncation

Results One subject’s data was excluded from the analysis because of skin artifact in the EMG signal. The data from the remaining 11 subjects was analyzed. The present experiment comprised a 2×2 factorial design with the factors of type of movement (internally generated or externally triggered), and truncation (truncated or not truncated). Figure 1 shows typical (median) trials for one subject.

There were no significant interactions between the two factors of type of movement and truncation with respect to rectified EMG activity (F(1,10)=2.951, p=.117) or the duration of EMG activity (F(1,10)=1.964, p=.191). In fact, EMG activity in both classes of truncation trials was slightly lower than in the pure internally generated and externally triggered trials, but this attenuation did not alter the basic difference between the characteristic EMG signatures of these classes of action.

521 Fig. 2 Rectified EMG activity (error bars are SE) in externally triggered and internally generated actions. EMG activity was greater for internally generated than for externally triggered actions

Statistics were performed on the mean of the trimmed RTs. A t-test revealed that truncation caused RTs to be on average 54.7 ms longer than RTs in the externally triggered movement condition (T(10)=−2.227, p