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Exp Brain ResDOI 10.1007/s00221-013-3411-x

REsEaRch aRtIclE

Concurrent adaptation of reactive saccades and hand pointing movements to equal and to opposite changes of target direction

Valentina Grigorova · Otmar Bock · Steliana Borisova

Received: 14 June 2012 / accepted: 7 January 2013 © springer-Verlag Berlin heidelberg 2013

Keywords Motor learning · Oculomotor · saccades · arm movement · Plasticity

Introduction

In daily life, hand movements to an object of interest are usually accompanied by saccadic eye movements. although eyes and hand are controlled by separate neural mechanisms, they do not act in complete isolation, since performance is enhanced when both motor systems aim at the same tar-get, and it is degraded when they aim at different targets (tipper et al. 2001; snyder 2002; lünenburger et al. 2000; Vercher et al. 1994; Niechwiej-szwedo et al. 2005). these findings support the existence a common internal represen-tation of the movement goal (Gielen and van asten 1990), possibly residing in neural networks that code the position both of the eyes and of the hand in the cerebellum (Miall et al. 2001), tectum (Werner et al. 1997a, b), premotor cortex (Pesaran et al. 2006a, b) and parietal cortex (andersen and Buneo 2002).

the adaptive plasticity of eye movements is typically evaluated with the double-step paradigm, where a visual target appears first in one location, and is displaced shortly thereafter. the displacement initially requires a response correction, but as adaptation progresses, the need for cor-rections gradually decreases. the double-step paradigm has been extensively used to adapt the amplitude and direction of saccades (Mclaughlin 1967; Deubel 1987; alahyane et al. 2004), but it also has been applied with success to adapt the amplitude and direction of aimed hand movements (Magescas and Prablanc 2006; Bock et al. 2008). this does not necessarily imply, however, that eye and hand adapta-tion is accomplished by a common neural mechanism. Even though both motor systems share a common representation

Abstract Eye as well as hand movements can adapt to double-step target displacements, but it is still controversial whether both motor systems use common or distinct adap-tive mechanisms. here, we posit that analyses of the con-current adaptation of both motor systems to equal versus different double-steps may provide more conclusive evi-dence than previous work about the transfer of adaptation from one motor system to the other. Forty subjects adapted to double-steps which called for a change of response direc-tion. the same (group s) or the opposite change (group O) was required for eyes and hand. Group ON equaled O, except that no visual feedback of the hand was provided. Groups E and h served as controls for eyes-only and hand-only adaptation, respectively. We found no differences between groups or motor systems when comparing s, E and h. adaptation was faster in O than in s, E and h, and faster still in ON. however, the magnitude of eye adaptation was much smaller in O and ON than in s, E and h. We con-clude that concurrent adaptation of eye and hand directions to opposite double-steps attenuates recalibration which, at least for the hand, is largely replaced by workaround strate-gies. the mechanisms for eye and hand adaptation there-fore seem to be coupled, in a way that hinders divergent recalibration of both motor systems. the possible neuronal substrate for our findings is discussed.

V. Grigorova (*) · s. Borisova Institute of Neurobiology, Bulgarian academy of science, sofia, Bulgariae-mail: valgri@bio.bas.bg

O. Bock Institute of Physiology and anatomy, German sport University, cologne, Germany

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of the movement goal and respond to the same adapta-tion paradigm, they may still utilize distinct adaptive mechanisms.

to find out whether eyes and hand rely on a common adaptive mechanism, previous studies tested for the transfer of adaptation from one motor system to the other: it was thought that substantial transfer would support the presence and negligible transfer the absence of a common mecha-nism. Unfortunately, the findings were ambiguous: no transfer was found from the amplitude of reactive saccades to that of hand movements (Kröller et al. 1999; cotti et al. 2007) but transfer was documented from the amplitude of voluntary saccades to that of hand movements (cotti et al. 2007) and from the direction of reactive saccades to that of hand movements (Bock et al. 2008). From this, it was concluded that depending on the context, eyes and hand can share a common—probably cortical (andersen and Buneo 2002; Pesaran et al. 2006a, b)—mechanism, but the eyes may alternatively rely on a proprietary subcortical mecha-nism (cotti et al. 2007; alahyane et al. 2007). this interpre-tation fits well with the view that adaptation is not a unitary phenomenon: When subjects are sequentially exposed to different distortions, they often must “unlearn” one distor-tion before learning the next, which has been interpreted as evidence for a common mechanism (lazar and van laer 1968; Bock et al. 2003; thomas and Bock 2010); however, subjects can also adapt to two or even four different distor-tions with no sign of interference when adequate contextual cues are provided, which has been attributed to the exist-ence of multiple parallel mechanisms (seidler et al. 2001; thomas and Bock 2012).

however, the discrepant findings on eye-hand transfer may not be related to the use of common versus distinct sensorimotor mechanisms. It has been suggested in the past that subjects’ performance in an adaptation task reflects not only the recalibration of sensorimotor mechanisms, but also the use of workaround strategies such as anticipations and reinterpretations of sensory or of motor signals. these strategies are thought to be situation-specific and short-lived (Redding and Wallace 1996; clower and Boussaoud 2000; Bock 2005) and thus to dissipate quickly—possibly even within a single trial (Wang and sainburg 2003)—when they become counter productive. strategies are counter-produc-tive during tests when aftereffects and for transfer to the opposite distortion, but remain useful during tests for trans-fer to another motor system. It therefore is conceivable that some earlier studies observed an eye-arm transfer of strat-egies, while other studies found no such transfer because strategies were not explicitly or implicitly encouraged or, alternatively, because strategies played a negligible role for one of the tested motor systems. the latter alternative is supported by the fact that eye-hand transfer was observed mostly with volitional rather than reactive saccades: while

reactive saccades are mainly controlled by the brainstem, voluntary saccades are controlled by neural circuitry that includes cortical structures (cotti et al. 2007; alahyane et al. 2007) and thus may well be linked to strategic pro-cesses as well.

It therefore seems conceivable that a common mecha-nism for both reactive saccade and hand movement adapta-tion is situated in sensorimotor paths responsible for their recalibration, which is much more stable and long lasting than strategy. We posit that, if such a common recalibra-tion mechanism exists, it should be activated when they adapt concurrently. the present study takes a new approach to distinguish between the existence a common versus two distinct mechanisms for eye and hand recalibration: rather than adapting one motor system and then testing for trans-fer to the other, we adapt both motor systems concurrently to opposite double-step regimes. If subjects’ performance on this task is much poorer than that of controls who adapt eyes and hand concurrently to one and the same double-step regime, this would be more compelling evidence for the existence of a common adaptive mechanism.

Methods

Forty healthy, right-handed subjects were divided equally into five groups (i.e., eight subjects per group). they signed their informed consent to this study, which was pre-approved by the Ethics committee of the Institute of Neurobiology. they were 27.5 ± 6.3 years old, had normal or corrected-to-normal vision and were naïve to eye and hand adaptation research. as in our earlier studies (e.g., Bock et al. 2008), subjects sat 40 cm in front of a 17″ flat computer screen, their head supported by a chinrest. In single-step trials, a target jumped from the monitor center 11 cm into the periph-ery, in one of eight randomly selected directions (0, 45, 90, 315°, where 0° denotes rightwards, and 90° upwards); the target returned to the center 760 ms later. In double-step tri-als, the target jumped in the same way, but its direction1 changed by −10/+10° (clockwise/counterclockwise) at the onset of the subjects’ primary saccade; the target returned to the center 640 ms later. the target for the hand was a gray square of 0.7 cm side length and that for the eyes was a black square of 0.5 cm side length. the black square remained centered within the gray one throughout all trials, except during the second target step of groups O and ON (see below).

subjects were instructed verbally to follow the targets with their eyes and/or hand. For hand movements, they held

1 saccade direction was defined, in analogy to pointing direction, as angular difference between primary target and saccade direction.

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a computer mouse in their right palm and moved it such as to displace a cursor on the screen. Mouse positions were mapped to cursor positions without a distortion, for exam-ple, a rightward movement of the mouse always led to a rightward movement of the cursor. We bypassed commer-cial mouse drivers to avoid their delays and averaging algo-rithms. horizontal and vertical eye position was registered by electrooculography (Dc-EOG) with a bandpass filter of 0.08–100 hz. the signal was sampled at 100 hz with a reso-lution of 0.01°/bit and was repeatedly calibrated throughout the experiment.

the experiment was subdivided into episodes of 20 tri-als, separated by short rest breaks. subjects from group S (“same”) started six baseline episodes of single-step trials. In the first two episodes, they responded both with their eyes and with their hand. In the subsequent four episodes, they responded either with their eyes only (hand resting in front of the body) or with their hand only (eyes fixating a mark in the screen center). the order of eyes-only and hand-only testing was counterbalanced across subjects. the baseline phase was followed by 30 adaptation episodes, which con-sisted of double-step trials: Black and gray targets changed their direction conjointly by −10° at the onset of the pri-mary saccade, and subjects followed them by combined eye and hand movements. Finally, it came six episodes of single-step trials, two eyes-only and two hand-only episodes in counterbalanced order, followed by two eye and hand epi-sodes. We introduced these episodes to test for aftereffects.

subjects from group O (“opposite”) received only four baseline episodes, as the episodes with combined eye and hand movements were omitted. During the subsequent 30 adaptation episodes, the black square was displaced at the onset of the primary saccade step by −10° and the gray square by +10°; subjects were asked to follow the black square with their eyes and the gray one with their hand. Next came five2 counter-adaptation episodes where the black square was displaced by +10° and the gray one by −10°; subjects again had to follow the black square with their eyes and the gray one with their hand, that is, they had to adapt both motor systems with opposite polarity than in the preceding 30 episodes. Finally, it came two episodes of eyes-only and two of hands-only single-step trials, in coun-terbalanced order.

Group ON (“opposite—no feedback”) differed from O only in that subjects moved the mouse without seeing a cursor, that is, visual feedback about hand movement was absent.

Group E followed the target with the eyes only and kept the hand still, while group H followed the target with the hand only and keep their gaze at the fixation mark in the

2 We thought five episodes were enough to estimate whether eye and hand adaptation differed.

screen center. Both groups were tested with two baseline episodes of single-step movements, followed by 30 adapta-tion episodes of double-step movements and then by two aftereffect episodes of single-step movements.

the collected eye and hand data were parameterized by interactive software that determined, for each trial:

• saccade direction: angular difference, in the screen plane, between first target step and primary saccade;

• hand direction: angular difference, in the screen plane, between first target step and hand movement 100 ms after each response onset, thus excluding the effects of feedback-based corrections;

• saccade latency: delay between first target step and onset of primary saccade;3

• hand latency: delay between first target step and onset of hand movement.

Responses with eye latencies >270 ms and hand laten-cies >400 ms were discarded, since they may be influenced by reprogramming toward the second step already at move-ment onset (Becker and Jürgens 1979; van sonderen et al. 1988). this was mainly the case in a few early double-step trials of group ON.

We then calculated the mean response direction for each subject, episode and motor system and adjusted for base-line differences by subtracting, from all episodes of a given subject and motor system, the mean of the initial two epi-sodes. the outcome was submitted to analyses of variance (aNOVas); to facilitate interpretation, hand directions from groups O and ON were sign inverted for these analyses, such that successful adaptation always corresponded to negative values.

Results

Figure 1 illustrates that eye and hand directions of groups s, h and E gradually changed during the adaptation phase with a similar time-course toward a similar plateau. this observation was confirmed by two-way aNOVas that com-pared (1) eye and hand adaptation in group s, (2) eye adap-tation in group E and hand adaptation in group h, (3) eye adaptation in groups s and E, as well as (4) hand adaptation in groups s and h. all analyses yielded a significant effect only for Episode,4 not for system, Group or the interaction

3 the registered eye movements consisted of a primary saccade typi-cally followed in double-step trials by a corrective saccade. here, we analyze only the reaction time and direction of primary saccades.4 the respective aNOVa outcomes were (F(29,377) = 5.68, p < 0.001); (F(29,377) = 4.6, p < 0.001); (F(29,377) = 5.4, p < 0.001) and (F(29,377) = 5.12, p < 0.001).

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term. the magnitude of eye adaptation, calculated from the last two episodes, was 65 and 59 % in groups s and E, respectively; the magnitude of hand adaptation was 51 and 57 % in groups s and h, respectively. We thus have no evidence that concurrent eye and hand adaptation to the same double-steps differs from eyes-only or hand-only adaptation.

Figure 2 shows that hand direction changed gradually in group O and abruptly in group ON, reaching a positive plateau as adequate for adaptation. Eye direction changed toward a negative plateau, which is again adequate, but the magnitude of change was small. three-way aNOVa yielded a significant effect for Episode (F(29,754) = 1.59, p < 0.05) and system (F(1,26) = 26.2, p < 0.001), but not for Group or any interaction term. the relative magnitude of eye adaptation was 11.5 and 28 % in groups O and ON, respectively; the magnitude of hand adaptation was 78 and

61.5 % in groups O and ON, respectively. thus, concurrent adaptation to opposite target steps was strongly attenuated for the eyes, but not for the hand.

at the onset of counter-adaptation in groups O and ON, eye and hand directions abruptly approached or even crossed the zero line and then changed as adequate for the new double-step regime (Fig. 2). this change was smaller than during the original adaptation for the hand, but not for the eyes. Indeed, aNOVas of the first five adaptation and all five counter-adaptation episodes (the latter with reversed sign) with the between factors Group (O, ON) and Order (original adaptation, counter-adaptation) and the within- factor Episode (1, …, 5) established a significant effect of Order (F(1,112) = 8.8, p < 0.01) and Episode (F(4,112) = 2.46, p < 0.05) for the hand data, but not for the eye data. the effect of Group and all interactions were non-significant for both motor systems.

Fig. 1 Eye and hand direc-tions during the baseline phase, during adaptation to double-step changes of target direction by −10°, and during the afteref-fect phase of group s (a) and of groups E and h (b). Each symbol is the across-subject mean of one episode, and each error bar the pertinent intersub-ject standard deviation. Note the similarity between all curves

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aftereffects in group s amounted to 37 % of the last two adaptation episodes when the eyes moved alone and to 52 % when the hand moved as well; they were also 52 % when the hand moved alone and 48 % when it moved together with the eyes. two-way aNOVa with the within-factors system (eye, hand) and combination (alone, together) yielded no significant effects of system or combination. aftereffects in group E were 50 % and in group h 41 %. One-way aNO-Vas yielded no significant differences between eye afteref-fects in groups s and E, nor between hand aftereffects in groups s and h. We therefore conclude that aftereffects were similar across the three groups, both motor systems and their combinations, averaging 48 %.

aftereffects in groups O and ON are difficult to interpret since they may reflect both the immediately preceding coun-ter-adaptation and/or the earlier adaptation. Nevertheless, it

is interesting to note that they were of equal polarity for both motor systems even though the respective distortions were of opposite polarity and that they were positive in O but negative in ON. after sign reversal in group ON, two-way aNOVa established no significant effects of Group or sys-tem but a significant constant (F(1,28) = 13.70; p < 0.001), that is, aftereffects were significantly different from zero. their average magnitude was 1.31°.

the baseline latency across all groups was shorter for the eyes (168 ± 25 ms) than for the hand (248 ± 53 ms), in accordance with the observations of others (Biguer et al. 1982; Pélisson et al. 1986; lünenburger et al. 2000). as Figs. 3 and 4 illustrate, eye and hand latencies of groups E and h and the eye latency of groups O and ON changed little during adaptation, while the hand latency of group s decreased by up to 23 ms, that of group O increased by up

Fig. 2 Eye and hand direc-tions during the baseline phase, during adaptation to double-step changes of target direction by −10° for the eyes and +10° for the hand, and during the cross-adaptation and afteref-fect phases of groups O (a) and ON (b). Each symbol is the across-subject mean of one episode, and each error bar the pertinent intersubject standard deviation. Note the differences between eyes and hand, and the early onset of adaptive change particularly in group ON

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to 70 ms, and that of group ON increased by up to 130 ms. the interval between second target step and hand movement onset thus increased to a maximum of 160 ms in group O and 290 ms in group ON. since the latter value is longer than 200 ms—the modification time of hand movements (van sonderen et al. 1988)—hand directions of group ON may reflect not only adaptive change, but in some episodes movement reprogramming as well.

Discussion

the present study dealt with the existence of common ver-sus distinct mechanisms for eye and hand adaptation to double-steps of target direction. Previous work addressed

this issue by evaluating the transfer of adaptation between motor systems; here, we argue that transfer studies may con-found adaptive recalibration and strategic adjustments and that analyses of concurrent versus separate adaptation may be more suitable.

When eyes and hand responded to the same double-step targets (group s), eye adaptation was comparable to hand adaptation; furthermore, both were comparable to the adap-tation of a single motor system (groups E and h). the same held for the aftereffects. thus, the mere fact of adapting two rather than a single motor system did not modify perfor-mance appreciably. Group s therefore serves as a control, asserting that the modifications observed in groups O and ON are not simply due to concurrency, but rather to the opposite sign of eye and hand adaptation.

Fig. 3 Eye and hand latencies of group s (a) and of groups E and h (b). Each symbol is the across-subject mean of one episode, and each error bar the pertinent intersubject standard deviation

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When eyes and hand responded to opposite double-step targets (groups O and ON), adaptation proceeded much faster than in the above groups, reached a similar plateau as in those groups for the hand, but a much lower plateau for the eyes. the latter finding is a sign of interference: eye adaptation deteriorated when the hand concurrently adapted to opposite rather than to the same double-steps. In accord-ance with our reasoning in the Introduction, we posit that the observed interference most likely emerged because both motor systems used a common adaptive mechanism. If they had used independent mechanisms, adaptation of one motor system should not be affected by adaptation of the other.

counter-adaptation in groups O and ON was remark-ably fast as well: Eyes and hand reflected the new dou-ble-step polarity already during the very first episodes,

which is much earlier than in previous studies on counter-adaptation (Bock et al. 2003; Miall et al. 2004; Wigmore et al. 2002). this quick change suggests, again following established arguments (Redding and Wallace 1996; clower and Boussaoud 2000; Bock et al. 2005), that the preced-ing adaptation phase of O and ON mainly reflected stra-tegic adjustments rather than adaptive recalibration. thus, summing up, we assume that exposing eyes and hand to opposite double-steps strongly attenuated adaptive recali-bration due to interference within a common mechanism and that at least for the hand, recalibration was replaced by strategies. the proposed contribution of strategies is supported by the increase in hand latencies during adap-tation: since strategic processes often involve cognition, they likely consume extra time.

Fig. 4 Eye and hand latencies of groups O (a) and ON (b). Each symbol is the across-subject mean of one episode, and each error bar the pertinent intersubject standard deviation. Note the increase in hand laten-cies during adaptation, mainly in group ON

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One possible reason for the strategic advantage of the hand over the eyes is that only hand movements can benefit from ongoing visual feedback. Group ON was introduced to scrutinize this view: if strategies are indeed strengthened by feedback, they should be attenuated in group ON to group O. Our data show that on the contrary, adaptive changes were even slightly more pronounced in group ON. From this, we conclude that the strategic advantage of the hand is probably not due to ongoing visual feedback.

It is established that eye and hand movements are pro-cessed in cortical (andersen and Buneo 2002; Pesaran et al. 2006a, b) as well as subcortical structures (Werner et al. 1997a, b; Miall et al. 2001). however, reactive saccades—like those elicited in the present study—seem to be mainly controlled by the brainstem (cotti et al. 2007; alahyane et al. 2007). there, the most likely candidates for adaptive recalibration are the superior colliculi (sc), which are associated not only with saccades (Desmurget et al. 1998, 2000; takeichi et al. 2007) but also with hand move-ments (Werner 1993; Werner et al. 1997a, b; stuphorn et al. 2000; lünenburger et al. 2000; Neggers and Bekkering 2002; courjon et al. 2004). the involvement of sc in adap-tive change is mainly deduced from the fact that saccadic adaptation is directionally tuned (Deubel 1987; Deubel 1995; Frens and van Opstal 1994; straube et al. 1997) as is double-step hand adaptation (schmitz et al. 2010) and that the tuning curves of both motor systems are remarkably similar to the “motor fields” of sc neurons (Frens and van Opstal 1997; Noto et al. 1999; schmitz et al. 2010).

Neggers and Bekkering (2002) studied concurrent eye and arm movements toward one common or two distinct targets and observed that the gaze always followed the tar-get intended for the hand. to interpret their finding, they proposed that saccade-related sc neurons are closely cou-pled to reach-related sc neurons and thus cannot control eye movements independently. If so, a possible interpreta-tion of the data from groups O and ON is that conflicting targets for eyes and hand suppress reach-related sc neurons via projections from the premotor (Werner et al. 1997a, b) and parietal cortex (asanuma et al. 1985), thus reducing the adaptive recalibration of hand movements and of reac-tive eye movements at the collicular level. hand but not eye adaptation can be substantially supported and even replaced by strategies, possibly utilizing adaptation-related circuitry in the parietal and prefrontal cortex (clower et al. 1996; Girgenrath et al. 2008).

summing up, we posit that a common mechanism for double-step adaptation of reactive saccade and hand movement directions is situated at a subcortical level, where it relies mainly on sc neurons, while an additional mechanism for double-step adaptation of hand move-ments is located at the cortical level. Eye and hand rec-alibration to the same double-steps can therefore proceed

in parallel at the sc level with no sign of interference, while eye and hand recalibration to opposite double-steps interferes at the sc level; the lack of recalibration of the hand, but not that of the eyes, is largely substituted by cortically mediated strategies. thus, the common mecha-nism for eye and hand adaptation works in a way that hin-ders divergent directional recalibration of the two motor systems.

Acknowledgments this work was supported by DFG exchange grant 436BUl113/148/0-1 and by DFG grant BO 649/8-5.

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