Functional independence of explicit and implicit motor adjustments

Consciousness and Cognition 18 (2009) 145–159

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Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog

Functional independence of explicit and implicit motor adjustments Sandra Sülzenbrück *, Herbert Heuer Leibniz Research Centre for Working Environment and Human Factors, Ardeystrasse 67, 44139 Dortmund, Germany

a r t i c l e

i n f o

Article history: Received 1 September 2008 Available online 10 January 2009

Keywords: Implicit learning Explicit learning Intentional learning Incidental learning Visuomotor transformations After-effects Motor adjustment

a b s t r a c t Adaptation to novel visuomotor transformations for example when navigating a cursor on a computer monitor by using a computer mouse, can be explicit or implicit. Explicit adjustments are made when people are informed about the occurrence and the type of a novel visuomotor transformation and intentionally modify their movements. Implicit adjustments, in contrast, are made without reportable knowledge of a novel visuomotor transformation and without a change intention. The relation of implicit adjustments to explicit adjustments needs further clarification. Here we show that these two types of adjustment occur at the same time and remain functionally independent. The size of total adjustment turned out to be the sum of explicit and implicit adjustments measured in isolation, even when both processes produce opposite outcomes. In perspective our results demonstrate that automatic, implicit processes of motor control are not superseded by intentional, explicit ones, but only superposed. Ó 2008 Elsevier Inc. All rights reserved.

1. Introduction Modern tools such as computers often transform human movements, most frequently of the hand, into visually perceived motions of objects, most frequently of a cursor on a computer monitor. Visuomotor transformations of hand movements into cursor motions can be chosen arbitrarily in principle. It has been shown that human brains adapt to different types of novel visuomotor transformations like prismatic displacements (Redding & Wallace, 2006; von Helmholtz, 1867), visuomotor rotations (Krakauer, Pine, Ghilardi, & Ghez, 2000; Tong, Wolpert, & Flanagan, 2002; Wang & Sainburg, 2005), novel visuomotor gains (Bock & Burghoff, 1997; Krakauer et al., 2000; Verwey & Heuer, 2007) or visuomotor delays (Stetson, Cui, Montague, & Eagleman, 2006). Adaptation to visuomotor transformations is not necessarily associated with awareness of the transformation or of the appropriate motor adjustment (Abeele & Bock, 2003; Buch, Young, & Contreras-Vidal, 2003; Klassen, Tong, & Flanagan, 2005; Knoblich & Kircher, 2004). Here we ask how these involuntary adjustments are related to intentional ones. Since Ungerleider and Mishkin (1982) seminal chapter, evidence has been accumulated to show that visual information can be used differently for perception and action. Perhaps the most influential theory is that of Milner and Goodale (1995). They posit the existence of two functionally and anatomically separated visual systems. The so-called ‘‘what path” is the ventral cortical stream from the primary visual cortex to the temporal cortex. It serves (conscious) perception. The so-called ‘‘how path”, on the other hand, links the primary visual cortex with the parietal cortex (dorsal stream). It serves the (unconscious) visual control of movements. Regarding the issue of intended and unintended adjustments to visuomotor transformations, two kinds of evidence for perception–action dissociations are particularly pertinent. The first kind of evidence shows that hand movements can be modified in response to stimuli that are not consciously perceived. The double-step paradigm exploits the fact that humans can be made unaware of the displacement of a visual object if this displacement is synchronized with a saccade. In this paradigm participants are asked to point at a target. During * Corresponding author. Fax: +49 (0)231 1084 340. E-mail address: [email protected] (S. Sülzenbrück). 1053-8100/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.concog.2008.12.001

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the saccade the target is displaced. Results of various experiments have shown that individuals are able to adjust their arm movements to reach to the new target position without becoming aware of the displacement of the target position or the correction of their own movement (Bridgeman, Kirsch, & Sperling, 1981; Goodale, Pélisson, & Prablanc, 1986; Prablanc & Martin, 1992). Similarly, when target displacements could be perceived, Castiello, Paulignan, and Jeannerod (1991) showed a change of hand trajectory already 100 ms after the target had been displaced, whereas only about 400 ms after the displacement awareness of a change of target position was signalled by the participants. The results of these studies show that during the execution of a goal-directed movement corrections occur which one is not aware of. This phenomenon has recently been referred to as ‘‘hand sight” (Rossetti, Pisella, & Pélisson, 2000). The second kind of evidence shows that hand movements can be corrected without humans becoming aware of these corrections. This has also been found with the double-step paradigm, but much more striking have been observations with an experimental paradigm originally developed by Nielsen (1963). Fourneret and Jeannerod (1998) asked their participants to draw straight lines on a digitizer. On a computer monitor they saw the lines they drew. In some trials the lines on the computer screen were grossly distorted in being curved to the left or right side. In these trials participants adjusted their drawing movements in the direction opposite to the distortion. When asked about the direction of their hand movement, participants showed poor conscious monitoring of them. In contrast to the large amount of research on dissociations between action and (conscious) perception, only little is known about the interactions between the respective systems (c.f. Rossetti & Revonsuo, 2000). Some studies investigated the influence of intentional processes on automatic movement corrections to changes in target positions. Participants in an experiment of Day and Lyon (2000) saw visual targets which changed their position at a randomly chosen time. Participants’ task was either to make an arm movement in the direction of the target movement or in the opposite direction. When movements in the opposite direction were required, there were two components in the trajectory of the arm. The late component depended on the intention of the participants, whereas the early component led into the wrong direction, that is, in the direction of the target. Pisella et al. (2000) constructed a conflict between automatic hand movements, the so-called ‘‘auto-pilot”, and intentional motor control. Their participants had to stop goal-oriented movements when the target position changed during execution. Results showed movement corrections in the direction of the new target position. These automatic corrections occurred between 200 and 240 ms after the target displacement, whereas intentional movement corrections were only executed after 240 ms. The authors concluded that the ‘‘auto-pilot” is not influenced by voluntary control. The relation between strategic (conscious) or explicit adjustments on the one hand and automatic or implicit adjustments on the other hand has perhaps been most extensively investigated for sequence learning. However, this research has not led to a definite conclusion about the role of explicit and implicit processes yet. There are at least three possible ways in which explicit and implicit processes can concur. These we shall describe in some detail because we shall examine three respective hypotheses for adjustments to visuomotor transformations. A first possibility is that one process replaces the other one. This implicates that explicit and implicit processes cannot coexist. For example, Willingham (1998) proposed in his ‘‘control-based learning theory” that during the execution of a movement in the conscious mode, strategic, and thus explicit, processes replace perceptual-motor integration processes, which are classified as implicit. This first hypothesis will be referred to as replacement hypothesis. A second possible kind of interaction of explicit and implicit processes is that one process emerges from the other. We will refer to it as emergence hypothesis. For example, Willingham and Goedert-Eschmann (1999) compared a group of participants informed about the sequence in a serial reaction time task with a group of participants not informed about the regularity of the sequence. After training, both groups completed a transfer block, where a new sequence or the learned sequence was tested. Participants were not informed about the occurrence of the learned sequence. The main result was that both groups showed reaction time benefits for the previously learned sequence and that they did not differ in the amount of these benefits. From this result the authors concluded that implicit learning occurred as a concomitant of explicit learning. According to a second assumption of Willingham’s ‘‘control based learning theory” (1998), processes of perceptual-motor integration and of sequencing are also tuned when strategic processes take active control of performance. By activating the same structures as implicit processes do, conscious strategic control tunes these processes passively. An imaging study by Willingham, Salidis, and Gabrieli (2002) further revealed that active brain regions of participants who learned a sequence with explicit information did not differ from activated regions of participants without any information about the regularity of the sequence. The fact that both groups did not differ in active brain regions was interpreted as procedural, implicit learning being the consequence of performance when learning the sequence explicitly. The conclusion that implicit learning is an emergent concomitant of explicit learning is not the only conclusion that can be drawn from these results. It is also possible that implicit processes were active quite independently of explicit learning. This leads us to our third alternative how explicit and implicit processes could concur: both processes operate independently from the very beginning of learning and produce a total amount of motor learning which is the sum of the separate contributions. This third hypothesis will be referred to as independence hypothesis. Arguments against the emergence hypothesis and in favour of the independence hypothesis can be found in several imaging studies. In these studies entirely different neural networks were activated when the serial reaction time task was executed as an implicit learning task than when the same task was executed with explicit information about the sequence of signals (Grafton, Hazeltine, & Ivry, 1995; Honda et al., 1998). If implicit and explicit processes differed only quantitatively, similar brain regions should be activated by both of them. So these findings are clearly inconsistent with the view that implicit pro-

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cesses are an emergent concomitant of explicit processes, but they are consistent with the assumption of functionally independent processes. Different from the findings on sequence learning, there are only few studies on the influence and the concurrence of explicit and implicit processes of adjustment to changes in visuomotor transformations. Some of the available results cannot be related to the three theoretical conceptions. For example, the finding that participants with declarative knowledge about the occurrence of a change in visuomotor rotation showed larger adjustments of movements than participants without declarative knowledge (Werner & Bock, 2007) does not reject any of the three hypotheses. However, data from a study recently reported by Mazzoni and Krakauer (2006) argue in favour of the independence hypothesis. Although the authors did not address this issue, their data revealed that when both explicit strategy use and automatic processes of perceptual-motor integration were activated, the resulting amount of adjustment to visuomotor rotations was the sum of adjustments caused by strategic and automatic processes separately. Such additivity of strategic and implicit adjustments was also postulated for prism adaptation by Redding and Wallace (1993). The goal of our experiments was to investigate which one of the three possible ways of concurrence of implicit and explicit processes of motor adjustment can be observed when adjustments to changes in visuomotor transformations are made. We investigated one particular type of adjustment to changes in visuomotor transformations, namely adjusting to changes in visuomotor gain, as it can be found when navigating a cursor by moving a computer mouse. The purpose of the first experiment was to compare the size of adjustment when only incidental motor adjustments are provoked and when explicit information about the occurrence of a change in visuomotor gain is presented. From the resulting incidental and intentional motor adjustments first conclusions concerning possible ways of concurrence could be drawn. On the one hand, the observation of larger adjustments with explicit information than without explicit information would be consistent with any of the three hypotheses. Larger explicit adjustments could replace or emerge out of smaller implicit ones or explicit and implicit adjustments could sum up. On the other hand, the observation of smaller adjustments with explicit information than without explicit information would only be consistent with the view that one type of process replaces the other one (even if this results in a smaller adjustment).

2. Experiment 1 2.1. Method 2.1.1. Participants Altogether 26 healthy, right-handed, normal-sighted participants (13 male, 13 female) volunteered for this study. Their age ranged between 19 and 29 years (mean: 23.6 years, SD: 2.8 years). They received 15 € or course credit for taking part. Each participant was assigned either to the incidental or the intentional group, with each group consisting of 13 participants. 2.1.2. Apparatus and task The experimental paradigm was adapted from one successfully tested before (Knoblich & Kircher, 2004). Participants were seated in front of a digitizer and faced a 17-in. computer monitor in about 60 cm distance. They were requested to draw circles on the digitizer with a pen held in their right hand. The position of the pen on the digitizer was represented on the monitor with a black background by the position of a cursor, a white or red circle of 4.2 mm diameter. Circles drawn on the digitizer were to be of such size that the circles of the cursor on the monitor were of constant size. Each trial started with a synchronization period in which participants had to follow a target which moved on a circular path with an individually adjusted comfortable speed (1810 ms per cycle on average). At the beginning of the continuation phase of each trial the visuomotor gain, that is, the relation between motion of the cursor on the computer monitor and movement of the pen on the digitizer, was 1:1 (phase 1). During 50% of the trials, a change of the visuomotor gain from 1:1 to 1.2:1 was introduced after 1–1.9 circles (depending on the onset of change, which was randomized) had been drawn, so that the radius of the circular path of the cursor on the monitor became 20% larger than the radius of the circles drawn on the digitizer (phase 2). To successfully perform the task, participants had to reduce the radius of the circles drawn on the digitizer appropriately. After one full circle in phase 2, the visuomotor gain was reset to 1:1 (phase 3). The trial was over after another 2.1–3 circles had been drawn in phase 3. The change of gain was sufficiently small not to be experienced, but sufficiently large to result in measurable incidental motor adjustments (Knoblich & Kircher, 2004). To elicit intentional adjustments, participants in the intentional group were explicitly instructed about the nature of the gain change and the proper motor adjustment before the test. In addition, each change of the visuomotor gain was cued by a change of the colour of the cursor from white to red. Participants in the incidental group received no information about the change of the visuomotor gain. For them the colour of the cursor was constant throughout the experiment. 2.1.3. Design At the start of the experiment, participants were presented a written instruction on the computer monitor. The instruction explained the course of the experiment, and for the intentional group the change in visuomotor gain was explained. Following the instruction, a practice phase was completed. Participants saw a white outline circle on the computer monitor (47.2 mm radius) with the centre in the middle of the screen. They had to guide the cursor along the outline circle, draw-

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ing circles of a constant size with a self-chosen comfortable speed. After five circles had been drawn, the template, the white outline circle, disappeared and participants had to continue drawing circular paths, maintaining the size and rate until 15 circles were completed. If the rate was too slow (more than 2500 ms per cycle) or too fast (less than 1100 ms per cycle), practice was repeated. The mean duration of the 6th–15th circle drawn during practice represented the individual comfortable speed, which was then used as the speed of the target to be followed in the synchronization periods of the regular trials, as described above. After completion of three experimental blocks with 10 randomized trials with and without gain change each, all participants were interviewed by the experimenter. Whereas participants in the intentional group were asked about the usefulness of the explicit instruction of the gain change for the adjustment of their movements, participants in the incidental group were asked whether they had become aware of the changes in visuomotor gain. The interview for the incidental group started with general questions (‘‘Did you notice anything during the test?”) and finished with a detailed description of the change of visuomotor gain. 2.1.4. Data analysis The position of the tip of the pen was recorded (60 Hz sampling frequency) as x–y coordinates of a fixed Cartesian coordinate system with its origin in the centre of the digitizer and the monitor. Each time series was low-pass filtered (fourthorder Butterworth, 2.5 Hz, dual-pass). Radii of circles drawn on the digitizer were determined for each point of the movement trajectory. From the coordinates of each point, its precursor, and its successor the coordinates of the centre as well as the radius of the circle, on which the three points were located, were computed. Thus a time series of radii was obtained for each trial. For each quadrant of a circular movement path, called segment, the radii were averaged. Segments were determined from the zero crossings of the first derivatives of the x and y coordinates with respect to time. The first and last segments of a trial were excluded from further analyses. Furthermore, a segment was excluded if it was too short (less than 15 data points), had a mean radius of more than 300 mm or a mean tangential velocity of less than 50 mm/s. These exclusion criteria were applied to account for strong deviations from a circular path or possible stand-stills. A trial was classified as valid and included in further analyses when there were at least three valid segments in phases before and during a change of visuomotor gain as well as at least seven valid segments in phase 3 after a change of gain. Three participants were excluded from further analyses, because they did not produce valid segments in at least one condition in at least one experimental block. For the other participants, mean radii of all segments were computed for the phases before and during the change of visuomotor gain and of the last four segments after the change. 2.1.5. Statistical analyses The differences between mean radii before and during change of gain were analyzed with a repeated measures analysis of variance with the between-participant factor group (intentional, incidental) and the within-participant factors block (1–3) and condition (change of gain, no change of gain). Greenhouse–Geisser corrections were applied when appropriate. 2.2. Results 2.2.1. Adjustment of radii Fig. 1 shows mean radii of circles drawn on the digitizer in trials with and without change of gain before (phase 1), during (phase 2) and after (phase 3) change of gain. Radii in phase 3 will be presented for all experiments, but statistical analyses will only include radii in phases 1 and 2. In general, radii in phase 3 of experimental trials were identical or quite similar to radii in control trials. There were only few exceptions, mainly after intentional adjustments. Results showed that participants adjusted their movements during the change of the visuomotor gain in both groups, but the size of adjustment was different. Participants in the intentional group reduced the radii of drawn circles by 7.9 mm (SD 5.2 mm) when the visuomotor gain was changed. This reduction differed significantly from the change in control trials without change of the visuomotor gain, F(1, 21) = 95.20, p < .001. Participants in the incidental group reduced the radii of drawn circles by 3.7 mm (SD 2.3 mm) when gain was changed. This reduction again differed significantly from the change in control trials without change of visuomotor gain, F(1, 21) = 26.82, p < .001. The difference in change of radii between trials with and without change of visuomotor gain in the intentional group was significantly larger than the corresponding difference in the incidental group, reflected in a significant interaction of group and condition, F(1, 21) = 12.02, p < .01. Furthermore, main effects of group, F(1, 21) = 13.64, p < .01, and condition, F(1, 21) = 112.97, p < .001, were significant. 2.2.2. Interview In an interview after the test six participants in the incidental group reported that they had become aware of the change in visuomotor gain, but only after the nature of gain change had been explained to them by the interviewer. After the first general question of the interview, none of these participants declared that they had experienced anything unusual. The exclusion of the six participants from the analysis did not change the resulting effects and the size of motor adjustments.

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Fig. 1. Mean radii of circles in the first experiment for participants of the intentional (a) and the incidental group (b) in trials with change of visuomotor gain in phase 2 and in control trials.

2.3. Discussion The results of the first experiment reveal that explicit knowledge about the occurrence of a change of visuomotor gain amplifies adjustments to this change. Incidental adjustments were only about half the size of adjustments observed in participants with explicit knowledge. Although six of the uninformed participants claimed that they had become aware of the change in visuomotor gain, this knowledge apparently did not influence the size of motor adjustments. However, it remains unclear to what extent these six participants really had experienced changes in visuomotor gain before being interviewed about them. With respect to the nature of the relation between explicit and implicit motor adjustments to changes of visuomotor gain, the findings are consistent with any of the three different hypotheses envisaged. With an explicit strategy, adjustments turned out to be larger than when adjustment was only implicit. In terms of the three hypotheses, (1) explicit, strategic motor adjustments could replace incidental adjustments and lead to stronger adjustments alone; (2) explicit adjustments could be just a stronger form of implicit adjustments; (3) explicit as well as implicit processes could occur simultaneously, combining their separate influences on motor adjustments. Only the finding of a smaller rather than a larger adjustment in the intentional than in the incidental group would have been consistent only with the replacement hypothesis and the additional assumption that explicit adjustments can be smaller than implicit ones. 3. Experiment 2 To learn more about the relationship between explicit and implicit motor adjustments, we investigated possible differences in the after-effects of the adjustments in participants with explicit information about the occurrence of a change in visuomotor gain and participants not informed about it. After-effects of adjustments to new visuomotor transformations have been found for prism adaptation (Redding & Wallace, 2006; von Helmholtz, 1867), visuomotor rotations (Heuer & Hegele, 2008a) and changes in visuomotor gain (Heuer & Hegele, 2008b). Here we asked whether after-effects are also produced when the change of visuomotor gain occurs for a quite short period of time, as it was the case in all our experiments. After-effects should show up as smaller drawn circles matched to visually presented circles in a post-test after trials with change of visuomotor gain than without change of visuomotor gain. More importantly, we asked for an eventual difference in after-effects depending on whether motor adjustments had been induced with or without explicit cues, that is, intentionally or incidentally. More specifically, same after-effects after intentional and incidental adjustments of different size would suggest a common component to both types of adjustment which gives rise to the after-effects and an additional component in explicitly cued adjustments that does not result in after-effects. If, however, explicit adjustments replaced implicit ones, the size of after-effects in the two groups should be rank-ordered according to the rank-order of the adjustments, or perhaps after-effects should be absent in the one group if one of the two types of adjustment does not give rise to after-effects. 3.1. Method 3.1.1. Participants All participants (n = 27) were healthy and right-handed and between 20 and 29 years old (mean: 23.6 years, SD: 2.1 years). The 12 male and 15 female participants received 20 € or course credit for volunteering. The intentional group was formed by 14 persons, whilst 13 participants added up to the incidental group.

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3.1.2. Apparatus and task Only minor changes were made to the apparatus compared to the first experiment. Instead of a black background of the monitor, a light grey background was used. The colour of the cursor was blue instead of white. The duration of each trial was expanded, with 2–2.8 circles drawn before change of gain and two full circles during change of gain. In some conditions cursor colour was changed from blue to red, indicating change of visuomotor gain for the intentional group. In contrast to the first experiment the visuomotor gain was not changed back to 1:1 after change of gain had occurred. Instead there was a short break after phase 2, during which participants had to write the German word for circle (‘‘Kreis”) in block letters. The purpose of this writing task was to disrupt the continuous circular movement before the post-test took place. In the subsequent post-test participants were requested to draw circles on the digitizer in a size which matched the size of target circles presented on the monitor. The target circles had one of three possible radii (39.33 mm, 47.20 mm or 56.64 mm). Posttests were performed under visual open-loop conditions, that is, the cursor which indicated the position of the pen on the digitizer was not shown. 3.1.3. Design The course of the experiment was basically the same as in Experiment 1. In each of five test blocks, 12 trials with and without change of visuomotor gain were completed (four trials with each of three circle sizes in the post-test). After the test trials, again all participants were interviewed as described for Experiment 1. 3.1.4. Data analysis Criteria to exclude segments were similar to those in Experiment 1. Only the minimal numbers of segments required in each phase were changed. A trial was included in further analyses when during the first two drawn circles (after the first segment had been deleted) there was at least one valid segment for each of the four quadrants of circles. During change of visuomotor gain as well as in post-tests, this criterion was the same for the last two drawn circles. Radii of valid segments were then averaged for each participant and each phase of a trial. 3.1.5. Statistical analyses For the analysis of adjustment to changes in visuomotor gain, the differences between mean radii of circles drawn before and during change of gain were analyzed with a repeated measures analysis of variance with the between-participant factor group (intentional, incidental) and the within-participant factors block (2–5), condition (change of gain, no change of gain), and size of the target circle in the post-test (39.33 mm, 47.20 mm or 56.64 mm radius). To analyse circle size in post-tests, the individual mean radii were analyzed with a repeated measures analyses of variance with the same factors as in the first analysis of this experiment. 3.2. Results 3.2.1. Adjustment of radii during change of visuomotor gain The changes of the radii from phase 1 to phase 2 replicated the findings of the first experiment in that the reduction was stronger in the intentional group than in the incidental group, 8.9 mm (SD 7.1 mm) vs. 6.1 mm (SD 6.1 mm). This was reflected in a significant interaction of group and condition, F(1, 25) = 15.14, p < .001. As in Experiment 1, significant main effects of group, F(1, 25) = 4.46, p < .05, and condition, F(1, 25) = 239.90, p < .001, were found. Furthermore there was a significant main effect of block, F(3, 75) = 4.56, p < .05, revealing a slight increase in the difference between control trials and experimental trials over the course of the experiment. A significant main effect of size of target circle, F(2, 50) = 3.74, p < .05, was also found. 3.2.2. Radii in post-tests In post-tests both groups drew smaller circles after a change of visuomotor gain than in control trials (Fig. 2). This was reflected in a main effect of condition, F(1, 25) = 40.64, p < .001. However, in contrast to the immediate adjustments of radii, the groups did not differ in their after-effects, indicated by the non-significant interaction effect of group and condition, F(1, 25) = .30, p > .20. In the intentional group the mean radius was 45.3 mm (SD 2.59 mm) in post-tests after trials with change of gain and 46.6 mm (SD 2.56 mm) after control trials. In the incidental group the mean radius was 50.3 mm (SD 2.75 mm) after trials with change of visuomotor gain and 51.6 mm (2.78 mm) after control trials. Furthermore, a trivial main effect of size of target circle was found, F(2, 50) = 75.77, p < .001. Finally, there was a significant interaction effect of group and block, F(3, 75) = 3.79, p < .05, with radii in the intentional group showing a linear decrease in the course of the experiment, whilst there was no such change in the incidental group. 3.2.3. Interview One participant in the incidental group stated that she had become aware of the change in visuomotor gain, but only after the nature of the change in gain had been explained by the interviewer. Omission of this participant from the data analysis did not affect the basic pattern of results.

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Fig. 2. Mean radii of circles in the second experiment during post-tests after trials with gain change and after control trials for participants of the intentional (a) and incidental group (b).

3.3. Discussion Even the short-duration motor adjustments to changes in visuomotor gain of the present experiments produced after-effects. More importantly, participants in both groups did not differ in the size of these after-effects. This finding is in contrast to the results on motor adjustment during the change of visuomotor gain. Here, participants in the intentional group showed a significantly larger decrease of the size of drawn circles than the participants in the incidental group. From this discrepancy we conclude that there are at least two processes, explicit and implicit motor adjustment, active during adjustment to the change of visuomotor gain in the intentional group, whereas only one of these processes, the implicit process, is active in the incidental group. The effects of the latter process persist and are expressed as after-effects. The results of Experiment 2 are not consistent with the replacement hypothesis, except with the additional ad hoc assumption that implicit and explicit adjustments of different sizes result in same after-effects. Nonetheless, the observed findings could be the result of the two other proposed combinations. According to the emergence hypothesis, only explicit processes would have been active during intentional adjustment to changes in visuomotor gain, but implicit processes would have been co-activated. The independence hypothesis holds that separate implicit and explicit processes were both active during intentional adjustment. The third experiment serves to distinguish between these hypotheses. 4. Experiment 3 Under the assumption that explicit and implicit adjustments are derived from separate processes, as it is proposed by the independence hypothesis, it should be possible to isolate them and also to combine them. Implicit adjustments occur in response to gain changes that remain unnoticed. Explicit adjustments occur in response to cues which signal gain changes. Combined adjustments then should occur when both a cue and a gain change (which remains unnoticed) are present. Provided that separate implicit and explicit adjustments do not interact, additive effects of the cue and the actual gain change should be observed. In contrast, additive effects are quite unexpected under the assumption that with explicit instructions implicit adjustments are just a concomitant of explicit ones. In this case there is no reason that implicit adjustments should be the same with and without explicit cues. The reason is that with explicit cues implicit adjustments should be derived from the explicit adjustments, whereas without explicit cues they should be triggered by the unnoticed change of the visuomotor gain. Additivity of adjustments based on explicit and implicit processes implies their functional independence in the sense that the presence of one process does not influence the outcome of the other process. In addition, for functionally independent processes one could expect that the individual explicit and implicit adjustments are uncorrelated. However, even though uncorrelated adjustments would perhaps strengthen the independence hypothesis, correlated adjustments do not constitute evidence against it. The reason is that even the outcomes of functionally independent processes can covary across individuals if there are inter-individual differences that affect both types of process, specifically explicit as well as implicit motor adjustments. 4.1. Method 4.1.1. Participants Altogether 24 healthy right-handed participants (12 male, 12 female) volunteered. They were between 19 and 31 years old (mean: 24.0 years, SD: 3.3 years) and received 15 € or course credit for taking part.

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4.1.2. Apparatus and task Apparatus and task were the same as in Experiment 2. Like in Experiment 1, in each trial there was phase 3 again, where gain had been changed back to 1:1, with a length of 1.2–3 drawn circles and no post-test. All participants were informed about the occurrence of a change in visuomotor gain. Amount of adjustment was measured in three experimental conditions and a control condition. Condition colour + gain change was identical to the experimental condition with change of visuomotor gain for the intentional group in the first experiment. In condition gain change only a change of visuomotor gain occurred in phase 2 of a trial which was not cued by a change of colour of the cursor. This condition was identical to the experimental condition with change of visuomotor gain for the incidental group in the first experiment and served to measure implicit adjustments. In condition colour change there was no change of visuomotor gain, but the colour of the cursor was changed in phase 2. Adaptive adjustments of the radii of drawn circles in this condition estimate pure intentional adjustments not confounded by eventual implicit adjustments. Note that by the experience of the participants trials with only colour change were not different from trials with both colour and gain change, and trials with only gain change were not different from control trials in which neither visuomotor gain nor colour of cursor was changed. 4.1.3. Design Again, the course of the experiment was as described for Experiment 1. All participants were interviewed after completing five blocks of 24 trials (six trials of each type). The goal of the interviews was to identify those participants who had become aware of the conditions where either colour change of the cursor or change in visuomotor gain was missing. 4.1.4. Data analysis Data were analyzed as in Experiment 2, with the additional criterion that a trial was valid when there was at least one valid segment for each quarter of a circle also during the last two drawn circles. Data from one participant had to be excluded from further analyses. 4.1.5. Statistical analysis The differences between mean radii before and during change of gain were analyzed with a repeated measures analysis of variance with the within-participant factors block (2–5), change of gain (change of gain, no change of gain), and change of cursor colour (change of cursor colour, no change of cursor colour). We computed the partial correlation between the individual mean adjustments in conditions gain change and colour change, controlling for changes in size of radii in control trials. In addition we computed the partial correlation between the individual sums of adjustments in conditions gain change and colour change and the adjustment in condition colour + gain change. 4.2. Results 4.2.1. Adjustment of radii In all three experimental conditions radii of drawn circles became smaller from phase 1 to 2 (Fig. 3). Adjustments were strongest when both the colour and the gain were changed (colour + gain change). Here the radii were reduced by 9.5 mm

Fig. 3. Mean radii of circles in the third experiment in trials with change of colour of the cursor and change of visuomotor gain in phase 2 (colour + gain change), change of visuomotor gain without change of colour of the cursor in phase 2 (gain change), no change of gain but change of colour of the cursor (colour change) in phase 2 and control trials without change of gain or change of colour of the cursor.

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(SD 7.2 mm) in phase 2. This reduction differed significantly from the change in control trials, which was 1.4 mm, F(1, 22) = 128.50, p < .001. When only the gain was changed (gain change), radii were reduced by 5.8 mm (SD 3.4 mm). This reduction again was significantly larger than the change in control trials, F(1, 22) = 309.96, p < .001. Finally, when only the colour was changed (colour change), radii were reduced by 5.2 mm (SD 7.7 mm), which differed significantly from the change in control trials, F(1, 22) = 26.12, p < .001. The reduction of radii in colour + gain change was significantly different from the reduction of radii in gain change, F(1, 22) = 22.13, p < .001 as well as from the reduction of radii in colour change, F(1, 22) = 131.83, p < .001. There was no significant difference in the reduction of radii between the conditions gain change and colour change, F(1, 22) = .33, p > .20. The comparison of the changes of the radii revealed significant main effects of change of gain, F(1, 22) = 238.99, p < .001, and change of colour, F(1, 22) = 24.92, p < .001, but no statistically significant interaction of these two factors, F(2, 44) = 0.19, p > .20. There was a significant partial correlation between the sum of mean individual adjustments in conditions gain change and colour change and the mean individual adjustment in colour + gain change of r = .92, p < .001. The partial correlation between mean individual adjustments in conditions gain change and colour change was significant as well, r = .44, p < .05. 4.2.2. Interview When asked after the test whether they had experienced anything unusual, five participants claimed that they had detected trials with missing gain change, whilst three other participants declared that they had become aware of trials in which gain was changed but not indicated by a change in colour of the cursor. When informed about the two experimental conditions not consistent with the given instruction, twelve more participants stated that they had noticed one of these conditions or both. Only three participants gave no indication at all that they had noticed the conditions where either gain change or colour change was absent. These participants did not differ in the size of implicit motor adjustment from those participants who had detected the missing colour change or gain change, but their explicit adjustments were somewhat larger, although not significantly so. 4.3. Discussion The additive effects of change of gain and change of colour of the cursor on the adjustment of the radii of circles drawn on the digitizer suggest that the total adjustment is the sum of functionally independent explicit and implicit components. The operation of the one kind of motor adjustment seems to be ignorant of whether or not the other kind of motor adjustment is present. Under the assumption that implicit adjustments are just a concomitant of explicit adjustments when these are present (emergence hypothesis), additive effects are quite unlikely. Further, if the colour change had induced explicit adjustments that replaced implicit ones (replacement hypothesis), intentional adjustments with and without gain change should not have differed in size. Additive effects of change of gain and change of colour showed up not only in the means. The high correlation between the individual sums of the separate effects and the combined effects indicates consistent additive effects for individual participants. In spite of the evidence of functionally independent processes, there was a modest negative correlation between the individual implicit and explicit adjustments. Even though this finding does not support the independence hypothesis, it does not constitute evidence against it.

5. Experiment 4 The results of Experiment 3 indicate that the independence hypothesis captures the relation between explicit and implicit motor adjustments, whereas the findings are hard to bring in line with the emergence hypothesis. A stronger argument against the emergence hypothesis would be provided by data which show qualitative differences in explicit and implicit adjustments. Therefore we created an experimental situation, where implicit and explicit motor adjustments would lead into directions opposite to each other. Experiment 4 involves opposite gain changes, increments as well as decrements, in combination with cued increments only for the intentional group. 5.1. Method 5.1.1. Participants All of the 41 participants (21 male, 20 female) were right-handed, normal-sighted individuals with their age ranging from 18 to 29 years (mean age: 23.4 years, SD: 2.8 years). They received 15 € or course credit for taking part. Each participant was assigned either to the incidental (n = 20) or the intentional group (n = 21). 5.1.2. Apparatus and task Apparatus and task were again the same as in Experiment 3. The amount of adjustment was measured in two experimental conditions and a control condition without change of gain. In the experimental condition increase of gain gain was changed from 1:1 to 1.1:1, therefore requiring a decrease of radii of drawn circles as it was the case in Experiments 1–3. In contrast, in the experimental condition decrease of gain visuomotor gain was changed from 1:1 to 0.9:1. To compensate

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for this change, the size of radii of drawn circles had to be increased. The intentional group was informed about the occurrence of a change in visuomotor gain from 1:1 to 1.1:1 before the experiment, and for them colour of the cursor changed from blue to red when the visuomotor gain was changed in either of both directions. They were not informed about the gain change to 0.9:1. Again, the incidental group was not informed about the occurrence of the change in visuomotor gain. 5.1.3. Design The course of the experiment was as described for Experiment 1. All participants completed five blocks of 20 trials each, which were composed of 10 control trials and five trials of each experimental condition in a random order. The purpose of the interview after the test was to identify those individuals in the incidental group who had become aware of the changes in visuomotor gain and those individuals in the intentional group who had become aware of the gain change opposite to the instructed change. 5.1.4. Data analysis Data were analyzed as in Experiment 3. Data from two participants in the intentional group had to be excluded from further analyses. 5.1.5. Statistical analysis The differences between mean radii before and during change of gain were analyzed with a repeated measures analysis of variance with the between-participant factor group (intentional, incidental) and the within-participant factors block (2–5) and condition (increase of gain, decrease of gain, no change of gain). 5.2. Results 5.2.1. Adjustment of radii Mean radii for all conditions are displayed in Fig. 4. In condition increase of gain results were as expected from Experiments 1 and 2. Both groups decreased the size of radii of drawn circles, but the amount of adjustment was different between groups. Radii were decreased by 7.8 mm (SD 4.9 mm) in the intentional group and by only 3.3 mm in the incidental group (SD 2.7 mm). These differences between radii before and during change in visuomotor gain were significantly different from the corresponding difference in control trials for the intentional group, F(1, 37) = 69.17, p < .001, as well as for the incidental group, F(1, 37) = 13.86, p < .001. The larger adjustment in the intentional group was significantly different from the adjustment in the incidental group, F(1, 37) = 11.76, p < .01. In condition decrease of gain a qualitative difference in adjustment between groups was found. Whilst the intentional group decreased the size of radii by 3.4 mm (SD 5.7 mm), there was an increase by 2.2 mm (SD 1.9 mm) in the incidental group. In the intentional group this change was almost significantly different from the corresponding difference in control trials, F(1, 37) = 3.81, p = .06. The failure to actually reach statistical significance was due to larger variations in the amount of adjustment. In the incidental group there was a highly significant difference between adjustment in this experimental condition and control trials, F(1, 37) = 11.75, p < .01. The adjustments in both groups differed significantly from each other, F(1, 37) = 16.12, p < .001. When tested separately for each group, adjustments in the experimental conditions were significantly different from each other in the intentional group, F(1, 37) = 86.17, p < .001, and in the incidental group, F(1, 37) = 143.39, p < .001.

Fig. 4. Mean radii of circles in the fourth experiment for participants of the intentional (a) and the incidental group (b) in trials with increase of visuomotor gain in phase 2 (increase of gain), decrease of visuomotor gain in phase 2 (decrease of gain) and in control trials.

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The different patterns of adjustments in both groups were reflected in a significant interaction of group and condition, F(2, 74) = 11.55, p < .001. Also the main effects of group, F(1, 37) = 13.58, p < .001, and condition, F(2, 74) = 60.23, p < .001, became significant, with the intentional group showing an overall larger negative adjustment, whereas the incidental group showed an averaged adjustment close to zero. Adjustments in the increase of gain condition were largest; in control trials they were smallest. 5.2.2. Interview None of the 20 participants in the incidental group claimed awareness of the changes in visuomotor gain before the nature of the change of gain was explained to them. After that, three participants stated that they had become aware of the changes. In the intentional group, two participants claimed that they had become aware of those trials where gain was changed in the opposite direction than the one instructed to them. After the experimenter had explained that in some trials an increase of radius was required, eight more participants stated that they had become aware of this fact. Reanalyzing the data without these participants did not change the basic pattern of results. Whilst there was essentially no change in the amount of adjustment in the incidental group, participants in the intentional group, who had not become aware of the trials not consistent with the instruction, showed larger decreases of radii in both experimental conditions than those who had become aware of these trials. Only in condition decrease of gain, this difference was significant, F(1, 17) = 6.04, p < .05. 5.3. Discussion We found opposite adjustments to gain increments and decrements when no explicit cues were presented. When both kinds of gain changes were combined with cues for gain increments, the size of the drawn circles was reduced accordingly. This reduction was stronger when the cue for a gain increment co-occurred with the actual increment than when it co-occurred with the actual decrement. The difference between both experimental conditions in the intentional group can be explained in two ways. On the one hand, consistent with the emergence hypothesis, explicit motor adjustments alone could have led to a decrease of radii. The difference between the experimental conditions would then be due to the absence or presence of the adjustment triggered by the actual increase of visuomotor gain rather than by the cue. On the other hand, the difference between experimental conditions in the intentional group could have been caused by an implicit increase of radii that was only overrun by a stronger explicit decrease, summing up to a smaller decrease of radii than when the actual gain increment took place. This would be inconsistent with the emergence hypothesis because implicit processes emerging out of explicit ones can only differ in size, but not in the direction of adjustment. The second explanation seems more likely, because in Experiment 3 we have shown the additivity of explicit and implicit adjustments when both types of process lead into the same direction. Still the question remains whether such additivity can also be found if explicit and implicit adjustments contradict each other. The purpose of our last experiment was to answer this question.

6. Experiment 5 This experiment serves to extend the claim that the implicit and explicit processes produce additive adjustments. In Experiment 3 additivity was shown for identical directions of adjustments. Here we investigated the possibility of additivity for opposite explicit and implicit adjustments. 6.1. Method 6.1.1. Participants Altogether, 24 right-handed and normal-sighted participants (12 male, 12 female) with their age ranging from 19 to 29 years (mean age: 23.1 years, SD: 3.1 years) volunteered for this experiment. They received 15 € or course credit for taking part. 6.1.2. Apparatus and task Apparatus and task were the same as in Experiment 4. Overall, there were five types of experimental and control trials. Three of the five experimental conditions were similar to those of Experiment 3, only with the difference that instead of a gain change to 1.2:1 a smaller change to 1.1:1 was realized as well as instructed for all participants. Condition colour change was identical to the same condition in Experiment 3. Condition colour + gain change will now be referred to as colour + gain change, increase, whilst condition gain change from Experiment 3 is now called increase of gain. The two new conditions are similar to those conditions in Experiment 4 for both groups where there was a decrease of visuomotor gain. Condition decrease of gain is the same as decrease of gain for the incidental group, whilst condition colour + gain change, decrease is the same as decrease of gain in the intentional group. 6.1.3. Design The course of the experiment was again as described for Experiment 1. Six blocks of 24 trials each (four trials of each experimental condition and control trials) had to be accomplished by each participant. Once more, an interview was

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conducted after the test with the purpose to identify those individuals who had become aware of the experimental conditions not consistent with the instruction. 6.1.4. Data analysis Data were analyzed as in Experiment 3. Data from one participant had to be excluded from further analyses. 6.1.5. Statistical analysis The differences between mean radii before and during change of gain were analyzed with a repeated measures analysis of variance with the within-participant factors block (2–6), change of gain (decrease of gain, increase of gain, no gain change), and change of cursor colour (change of cursor colour, no change of cursor colour). Partial correlations, controlling for changes of radii in control trials, were computed between mean individual adjustments in gain change, increase and colour change as well as between mean individual adjustments in gain change, decrease and colour change. In addition partial correlations were obtained between the sums of mean individual adjustments in gain change, increase and colour change and the mean individual adjustments in colour + gain change, increase as well as between the sums of mean individual adjustments in gain change, decrease and colour change and the mean individual adjustments in colour + gain change, decrease. 6.2. Results 6.2.1. Adjustment of radii As Fig. 5 depicts, results for conditions with increased gain factor were similar to those found in Experiment 3. Whereas adjustment was strongest and significantly different from the corresponding changes in control trials, F(1, 22) = 63.64, p < .001, in condition colour + gain change, increase with 9.3 mm (SD 4.1 mm), adjustment was significantly smaller in condition increase of gain with only 4.2 mm (SD 1.6 mm), but still significantly different from changes in control trials, F(1, 22) = 59.75, p < .001. The difference in adjustment between these two conditions was statistically significant, F(1, 22) = 22.78, p < .001. In condition colour change there was also a decrease of drawn radii of 6.8 mm (SD 4.3 mm), that was significantly different from changes in control trials, F(1, 22) = 31.05, p < .001. This finding was in line with the results of Experiment 3. When visuomotor gain was decreased, there were qualitative differences in motor adjustment depending on whether the colour cue was present or absent. In condition colour + gain change, decrease radii were decreased by 4.2 mm (SD 5.3 mm), which was significantly different from changes in control trials, F(1, 22) = 5.00, p < .05. In contrast, in condition decrease of gain radii were increased by 1.3 mm (SD 2.0 mm), which was also significantly different from changes in control trials, F(1, 22) = 81.31, p < .001. Adjustment between both experimental conditions differed significantly, F(1, 22) = 20. 48, p < .001. Like in Experiment 3, we found significant main effects of change of gain, F(2, 44) = 133.61, p < .001, as well as of change of cursor colour, F(1, 22) = 24.85, p < .001, but no statistically significant interaction effect between those factors, F(2, 44) = .75, p > .20. Thus the effects were additive. There were significant partial correlations between the sums of mean individual adjustments in gain change, increase and colour change and the mean individual adjustments in colour + gain change, increase, r = .93, p < .001, as well as between the sums of mean individual adjustments in gain change, decrease and colour change and the mean individual adjustments in colour + gain change, decrease, r = .94, p < .001. As in Experiment 3, there was a significant partial correlation between adjust-

Fig. 5. Mean radii of circles in the fifth experiment in trials with change of colour of the cursor and an increase of visuomotor gain in phase 2 (colour + gain change, increase), change of colour of the cursor and a decrease of visuomotor gain in phase 2 (colour + gain change, decrease), increase of visuomotor gain without change of colour of the cursor in phase 2 (increase of gain), decrease of visuomotor gain without change of colour of the cursor in phase 2 (decrease of gain), no change of gain but change of colour of the cursor (colour change) in phase 2 and control trials without change of gain or change of colour of the cursor.

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ments in colour change and gain change, increase of r = change, decrease was only r = .19, p > .20.

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.47, p < .05. The partial correlation between colour change and gain

6.2.2. Interview Four participants stated that they had become aware of the need to draw larger circles, of the change of gain without the cue or of the change of cursor colour not accompanied by a change in visuomotor gain. After the experimenter had informed participants about the occurrence of the experimental trials not consistent with the instruction, 13 more participants claimed that they had become aware of at least one of these three types of condition. Only six participants had not become aware of any of them. Analyzing the data of only these six participants led to similar effects as those found for all participants. 6.3. Discussion The additivity of explicit and implicit motor adjustments, which had been shown in Experiment 3 for adjustments in the same direction, was also found when explicit and implicit motor adjustments were opposed to each other. Again the correlations reveal that the additivity was highly consistent across individual participants, both with congruent and incongruent explicit and implicit adjustments. The emergence hypothesis, which is incompatible with the observation of opposite concurrent explicit and implicit motor adjustments, has to be dismissed accordingly. As in Experiment 3, there was a negative correlation between the individual implicit and explicit adjustments. However, this correlation was statistically significant only for adjustments in the same direction, but not for adjustments in opposite directions. These data do not represent evidence in favour of the independence hypothesis, but neither do they provide evidence against it.

7. General discussion As it was proposed for different types of changes in visuomotor transformations (Abeele & Bock, 2003; Buch et al., 2003; Klassen et al., 2005; Knoblich & Kircher, 2004), our data show that the human brain can adapt to small changes in visuomotor gain without the person’s awareness of the changes in gain or in their movements. Similar implicit motor adjustments of the hand trajectory have been found with other paradigms as well (Bridgeman et al., 1981; Castiello et al., 1991; Fourneret & Jeannerod, 1998; Goodale et al., 1986; Prablanc & Martin, 1992), and they can also be referred to as ‘‘hand sight” (Rossetti et al., 2000). Providing explicit knowledge about the occurrence of changes in visuomotor gain led to stronger adjustments compared with the implicit ones. This beneficial effect of intentional modifications is in line with findings from other areas of motorlearning research (Curran & Keele, 1993; Werner & Bock, 2007; Willingham, Nissen, & Bullemer, 1989), but it is not trivial. A large body of research exists concerned with so-called choking under pressure, a decrement in performance when the actor wants to perform the best (Baumeister, 1984; Beilock & Carr, 2001; Lewis & Lindner, 1997). One way to explain this phenomenon is that attention is focussed on the execution of a well-learned or proceduralized skill, which normally would run unattended. In that case explicit processes could interfere with implicit processes, e.g. because the involvement of attention generally leads to a slowing of action execution. Since there was no time pressure to perform the task we used in our experiments, interference of explicit with implicit processes because of their slowness was unlikely to occur. With the basic finding of adjustments based on explicit knowledge being larger than implicit adjustments, the question arose in which way implicit and explicit motor adjustments concur. The main conclusion from our experiments is that implicit and explicit motor adjustments can occur in parallel and functionally independent of each other, consistent with the independence hypothesis, even if they lead to opposite directions of motor adjustment. This conclusion contradicts the view that strategic processes replace perceptual-motor integration during motor control (replacement hypothesis) or that implicit motor processes emerge from explicit processes (emergence hypothesis, cf. Willingham, 1998). Our findings are in line with findings of a cooperation of automatic and strategic processes during adaptation to prismatic displacements (Redding & Wallace, 1993). In addition, the data of Mazzoni and Krakauer (2006) suggest that additivity of explicit and implicit processes is not restricted to adjustments to changes in visuomotor gain, but also occurs in learning new visuomotor rotations. Our results are also consistent with observations reported by Day and Lyon (2000) as well as by Pisella et al. (2000) of automatic hand movements which occur independently of voluntary control. Further evidence of independent explicit and implicit processes can be found in several imaging studies. There it was shown that different neural networks were activated when the serial reaction time task was executed as an implicit learning task than when the same task was executed in an explicit mode (Grafton et al., 1995; Honda et al., 1998). Our notion of functional independence of explicit and implicit processes holds that the individual motor adjustments, which result from explicit and implicit processes, are not changed when the second process is active. We found this type of independence in both experiments in which explicit and implicit adjustments were measured separately, both in the means – as indicated by additive effects in analyses of variance – and in the individual adjustments – as indicated by the high and significant correlations between the sums of adjustments in the separate conditions and the adjustment in the combined condition.

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At first glance our conclusion of functional independence seems to be rejected by the negative correlation between the individual implicit and explicit adjustments. However, such correlations are consistent with functional independence and can be attributed to a third factor which varies across individuals and is related to both types of adjustment. Although we have no convincing evidence on the nature of such a third factor, individual sensitivity for circle sizes is a candidate. Participants with low sensitivity would need only small implicit adjustments to compensate a discrepancy between the radius of the seen circular motion and the remembered target radius. On the other hand, they would need a relatively strong explicit adjustment to note that the radius of the circular motion has actually been changed. Of course, such a difference in sensitivity should be (at least partially) common to the registration of radius changes for motor adjustments and for (conscious) perception. In addition, sensitivity for increases and decreases of radii might not be perfectly correlated across individuals, so that the negative correlation between explicit and implicit adjustments is smaller and non-significant when both types of process lead into opposite directions. Besides the main conclusion of independence, the results of our experiments allow a further characterization of explicit and implicit processes. The finding that the intentional and the incidental group produced same sized after-effects in spite of different immediate adjustments suggests that implicit adjustments were the same in both groups. Only implicit adjustments should be related to a modification of an internal model (Wolpert & Kawato, 1998), and therefore learning of the new visuomotor transformation which results in after-effects. In the intentional group an explicit adjustment was superposed on the implicit one, but this adjustment was strategic and not related to the modification of an internal model. Therefore it was not reflected in after-effects. A consequence of this difference between implicit and explicit adjustments to visuomotor transformations should be that only implicit adjustments establish new references or new expectations against which actual feedback is compared when judgements of self-agency are required (e.g. Metcalfe & Greene, 2007; Sato & Yasuda, 2005). Further information concerning the nature of explicit and implicit adjustments can be obtained when their individual variability is examined. Throughout all five experiments, the standard deviations were consistently smaller for implicit than for explicit adjustments, which suggests that the implicit process is rather uniform and barely affected by inter-individual differences. Explicit, intentional motor adjustments, in contrast, are sensitive to individual variations of adjustment strategies. Although in the present experiments explicit and implicit adjustments were additive, suggesting functionally independent processes, it should be noted that even functionally independent processes can produce interacting effects. Interactions between explicit and implicit adjustments can arise from the environmental variables which trigger both types of process. For example, implicit adjustments occur in response to gain changes that remain unnoticed, whereas explicit adjustments occur in response to cues which signal gain changes. When a change of visuomotor gain is cued, intentional motor adjustments occur that may mask the small changes in the relation between hand movements and resulting movements of the cursor on the monitor, therefore eliminating or at least diminishing the basis for the implicit motor adjustments. Such interaction effects between strategic processes and automatic processes of perceptual-motor recalibration can be found in prism adaptation (Redding & Wallace, 1993). Thus, the additivity observed in the present experiments is likely to be subject to boundary conditions. A further limitation of our results concerns the duration of change of visuomotor gain and therefore a limited amount of time for motor adjustments. Since we only investigated the concurrence of explicit and implicit motor adjustments in the course of short periods of time, no general conclusions can be drawn concerning long-term adjustments. Implicit adjustments in our experiments were only about half the size required to compensate the change in visuomotor gain. In an unpublished experiment, we doubled the duration of change of gain and found that the implicit adjustment came close to completely compensating the change in visuomotor gain. However, even in this condition, cueing the change in visuomotor gain led to an additional explicit motor adjustment. In all experiments in which the adjustment to changes in visuomotor gain was compared for the intentional and the incidental group (Experiments 1, 2, 4), significant main effects of the factor group were found. Radii in the intentional group were overall smaller than radii in the incidental group. Since assignment to groups was random, this main effect had to be caused by the experimental manipulation. A clue to the cause of this phenomenon can be found in the radii in the last phase of each trial where visuomotor gain had been changed back to 1:1. In the incidental groups the radii returned to the level of the control trials in this phase. In the intentional groups, in contrast, radii did not return to the level of control trials. This difference at the end of each trial could have partially survived until the next trial, therefore resulting in overall smaller radii in the intentional group than in the incidental group even in the first phases of each trial. Taken together, our findings show that implicit adjustments of movements to novel visuomotor transformations are neither replaced by strategic intentional adjustments nor emerge from explicit motor processes. Instead, both types of adaptive processes co-exist and remain functionally independent so that their outcomes are additive and independent of whether or not the other kind of process is present. Thus, even when we intentionally change movement characteristics to adjust to a new visuomotor transformation, unintended adjustments occur in addition. Acknowledgments We thank Petra Wallmeyer and Eckhard Rückemann for running the experiments.

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References Abeele, S., & Bock, O. (2003). Transfer of sensorimotor adaptation between different movement categories. Experimental Brain Research, 148, 128–132. Baumeister, R. F. (1984). Choking under pressure: Self-consciousness and paradoxical effects of incentives on skillful performance. Journal of Personality and Social Psychology, 46, 610–620. Beilock, S. L., & Carr, T. H. (2001). On the fragility of skilled performance: What governs choking under pressure? Journal of Experimental Psychology: General, 130, 701–725. Bock, O., & Burghoff, M. (1997). Visuo-motor adaptation: Evidence for a distributed amplitude control system. Behavioral Brain Research, 89, 267–273. Bridgeman, B., Kirsch, M., & Sperling, A. (1981). Segregation of cognitive and motor aspects of visual function using induced motion. Perception and Psychophysics, 29, 336–342. Buch, E. R., Young, S., & Contreras-Vidal, J. L. (2003). Visuomotor adaptation in normal aging. Learning and Memory, 10, 55–63. Castiello, U., Paulignan, Y., & Jeannerod, M. (1991). Temporal dissociation of motor responses and subjective awareness. A study in normal subjects. Brain, 114, 2639–2655. Curran, T., & Keele, S. W. (1993). Attentional and nonattentional forms of sequence learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 19, 189–202. Day, B. I., & Lyon, I. N. (2000). Voluntary modification of automatic arm movements evoked by motion of a visual target. Experimental Brain Research, 130, 159–168. Fourneret, P., & Jeannerod, M. (1998). Limited conscious monitoring of motor performance in normal subjects. Neuropsychologia, 36, 1133–1140. Goodale, M. A., Pélisson, D., & Prablanc, C. (1986). Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature, 320, 748–749. Grafton, S. T., Hazeltine, E., & Ivry, R. (1995). Functional mapping of sequence learning in normal humans. Journal of Cognitive Neuroscience, 7, 497–510. Heuer, H., & Hegele, M. (2008a). Adaptation to direction-dependent visuo-motor rotations and its decay in younger and older adults. Acta Psychologica, 127, 369–381. Heuer, H., & Hegele, M. (2008b). Constraints on visuo-motor adaptation depend on the type of visual feedback during practice. Experimental Brain Research, 185, 101–110. Honda, M., Deiber, M. P., Ibanez, V., Pascual-Leone, A., Zhuang, P., & Hallett, M. (1998). Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. Brain, 121, 2159–2173. Klassen, J., Tong, C., & Flanagan, J. R. (2005). Learning and recall of incremental kinematic and dynamic sensorimotor transformations. Experimental Brain Research, 164, 250–259. Knoblich, G., & Kircher, T. T. J. (2004). Deceiving oneself about being in control: Conscious detection of changes in visuo-motor coupling. Journal of Experimental Psychology: Human Perception and Performance, 30, 657–666. Krakauer, J. W., Pine, Z. M., Ghilardi, M.-F., & Ghez, C. (2000). Learning of visuomotor transformations for vectorial planning of reaching trajectories. Journal of Neuroscience, 20, 8916–8924. Lewis, B., & Lindner, D. (1997). Thinking about choking? Attentional processes and paradoxical performance. Personality and Social Psychology Bulletin, 23, 937–944. Mazzoni, P., & Krakauer, J. W. (2006). An implicit plan overrides an explicit strategy during visuomotor adaptation. Journal of Neuroscience, 26, 3642–3645. Metcalfe, J., & Greene, M. J. (2007). Metacognition of agency. Journal of Experimental Psychology: General, 136, 184–199. Milner, A. D., & Goodale, M. A. (1995). The visual brain in action. Oxford: Oxford University Press. Nielsen, T. I. (1963). Volition: A new experimental approach. Scandinavian Journal of Psychology, 4, 225–230. Pisella, L., Gréa, H., Tilikete, C., Vighetto, A., Desmurget, M., Rode, G., et al (2000). An ‘automatic pilot’ for the hand in human posterior parietal cortex: Toward reinterpreting optic ataxia. Nature Neuroscience, 3, 729–736. Prablanc, C., & Martin, O. (1992). Automatic control during hand reaching at undetected two-dimensional target displacements. Journal of Neurophysiology, 67, 455–469. Redding, G. M., & Wallace, B. (1993). Adaptive coordination and alignment of eye and hand. Journal of Motor Behavior, 25, 75–88. Redding, G. M., & Wallace, B. (2006). Generalization of prism adaptation. Journal of Experimental Psychology: Human Perception and Performance, 32, 1006–1022. Rossetti, Y., Pisella, L., & Pélisson, Y. (2000). Eye blindness and hand sight: Temporal aspects of visuo-motor processing. Visual Cognition, 7, 785–809. Rossetti, Y., & Revonsuo, A. (Eds.). (2000). Beyond dissociation interaction between dissociated implicit and explicit processing. Amsterdam: John Benjamins. Sato, A., & Yasuda, A. (2005). Illusion of sense of self-agency: Discrepancy between the predicted and actual sensory consequences of actions modulates the sense of self-agency, but not the sense of self-ownership. Cognition, 94, 241–255. Stetson, C., Cui, X., Montague, P. R., & Eagleman, D. M. (2006). Motor-sensory recalibration leads to an illusory reversal of action and sensation. Neuron, 51, 651–659. Tong, C., Wolpert, D. M., & Flanagan, J. R. (2002). Kinematics and dynamics are not represented independently in motor working memory: Evidence from an interference study. Journal of Neuroscience, 22, 1108–1113. Ungerleider, L. G., & Mishkin, M. (1982). Two cortical visual systems. In D. J. Ingle, M. A. Goodale, & R. J. W. Mansfield (Eds.), Analysis of visual behavior (pp. 549–586). Cambridge, Mass: MIT Press. Verwey, W. B., & Heuer, H. (2007). Nonlinear visuomotor transformations: Locus and modularity. Quarterly Journal of Experimental Psychology, 60, 1629–1659. von Helmholtz, H. (1867). Handbuch der physiologischen Optik. Voss: Leipzig. Wang, J., & Sainburg, R. L. (2005). Adaptation to visuomotor rotations remaps movement vectors, not final positions. Journal of Neuroscience, 25, 4024–4030. Werner, S., & Bock, O. (2007). Effects of variable practice and declarative knowledge on sensorimotor adaptation to rotated visual feedback. Experimental Brain Research, 178, 554–559. Willingham, D. B. (1998). A neuropsychological theory of motor skill learning. Psychological Review, 105, 558–584. Willingham, D. B., & Goedert-Eschmann, K. (1999). The relation between implicit and explicit learning: Evidence for parallel development. Psychological Science, 10, 531–534. Willingham, D. B., Nissen, M., & Bullemer, P. (1989). On the development of procedural knowledge. Journal of Experimental Psychology: Learning, Memory, and Cognition, 15, 1047–1060. Willingham, D. B., Salidis, J., & Gabrieli, J. D. E. (2002). Direct comparison of neural systems mediating conscious and unconscious skill learning. Journal of Neurophysiology, 88, 1451–1460. Wolpert, D. M., & Kawato, M. (1998). Multiple paired forward and inverse models for motor control. Neural Networks, 11, 1317–1329.