Adapting terminology: clarifying prism adaptation vocabulary, concepts, and methods.

When individuals are exposed to a constant change of the interplay with their environment, they are able to develop compensatory alterations of visuo-motor coordination in order to counteract the perturbation. Prism adaptation (PA) is a very simple tool that has been used for several decades to investigate adaptive processes. However, the specific terminology used in PA literature has continuously evolved and is still subjected to broad inconsistency. Growing confusion about the choice of terms used to describe specific processes and methods has yielded the critical need for clarifying the adaptation vocabulary. The aim of this terminology review is to consider and to describe the most common terms used in PA literature in order to ensure more consistent communication in future research. On the basis of a descriptive examination of previous studies on PA, we provide specification for each term, indicating whether it refers to a classical term in PA literature, and whether it is recommended or should be used with particular attention. This glossary represents a useful instrument to both new readers and experts in the field of PA in order to facilitate unambiguous communication and consensual comparisons between individual investigations. Recommendations for the use of consistent paradigms and reliable vocabulary are provided for future investigations, in both basic and clinical research.

Pointing to double-step visual stimuli from a standing position: very short latency (express) corrections are observed in upper and lower limbs and may not require cortical involvement.

How fast can we correct a planned movement following an unexpected target jump? Subjects, starting in an upright standing position, were required to point to a target that randomly and unexpectedly jumps forward to a constant spatial location. Rapid motor corrections in the upper and lower limbs, with latency responses of less than 100 ms, were revealed by contrasting electromyographic activities in perturbed and unperturbed trials. The earliest responses were observed primarily in the anterior section of the deltoïdus anterior (shoulder) and the tibialis anterior (leg) muscles. Our findings indicate that visual on-going movement corrections may be accomplished via fast loops at the level of the upper and lower limbs and may not require cortical involvement.

Automatic drive of limb motor plasticity.

The ability to perform accurate limb movements may require learning mechanisms that continually tune the motor system. In the current study, we isolate a form of pure limb motor plasticity. Participants reached to targets that were turned off just after the onset of an initial eye movement, reappearing at a new location at the end of the reaching movement. In contrast to classical prism or virtual reality paradigms, our task eliminated sensory adaptation by always maintaining a congruency between the seen and felt limb position. We also minimized awareness and potential adaptation processes on the basis of volitional strategies by progressively increasing the size of the target perturbations. In this manner, our adaptation procedure mimicked conditions used to study saccadic adaptation. The results indicated that adaptation under these conditions led to a robust after-effect that generalized to a large range of movements within the workspace. This fully natural, nonimposed generalization of adaptation is not expressed in a spatial coordinate system, but more likely in a joint-centered coordinate space.

Functional anatomy of nonvisual feedback loops during reaching: a positron emission tomography study.

Reaching movements performed without vision of the moving limb are continuously monitored, during their execution, by feedback loops (designated nonvisual). In this study, we investigated the functional anatomy of these nonvisual loops using positron emission tomography (PET). Seven subjects had to "look at" (eye) or "look and point to" (eye-arm) visual targets whose location either remained stationary or changed undetectably during the ocular saccade (when vision is suppressed). Slightly changing the target location during gaze shift causes an increase in the amount of correction to be generated. Functional anatomy of nonvisual feedback loops was identified by comparing the reaching condition involving large corrections (jump) with the reaching condition involving small corrections (stationary), after subtracting the activations associated with saccadic movements and hand movement planning [(eye-arm-jumping minus eye-jumping) minus (eye-arm-stationary minus eye-stationary)]. Behavioral data confirmed that the subjects were both accurate at reaching to the stationary targets and able to update their movement smoothly and early in response to the target jump. PET difference images showed that these corrections were mediated by a restricted network involving the left posterior parietal cortex, the right anterior intermediate cerebellum, and the left primary motor cortex. These results are consistent with our knowledge of the functional properties of these areas and more generally with models emphasizing parietal-cerebellar circuits for processing a dynamic motor error signal.

Postural invariance in three-dimensional reaching and grasping movements.

The question of whether the final arm posture to be reached is determined in advance during prehension movements remains widely debated. To address this issue, we designed a psychophysical experiment in which human subjects were instructed to reach and grasp, with their right arm, a small sphere presented at various locations. In some trials the sphere remained stationary, while in others (the perturbed trials) it suddenly jumped, at movement onset, to a new unpredictable position. Our data indicate that the final configuration of the upper limb is highly predictable for a given location of the sphere. For movements directed at stationary objects, the variability of the final arm posture was very small in relation to the variability allowed by joint redundancy. For movements directed at "jumping" objects, the initial motor response was quickly amended, allowing an accurate grasp. The final arm posture reached at the end of the perturbed trials was neither different from nor more variable than the final arm posture reached at the end of the corresponding stationary trials (i.e. the trials sharing the same final object location). This latter result is not trivial, considering both joint redundancy and the motor reorganization imposed by the change in sphere location. In contrast to earlier observations, our data cannot be accounted for by biomechanical or functional factors. Indeed, the spherical object used in the present study did not constrain the final arm configuration or the hand trajectory. When considered together, our data support the idea that the final posture to be reached is planned in advance and used as a control variable by the central nervous system.

Functional adaptation of reactive saccades in humans: a PET study.

It is known that the saccadic system shows adaptive changes when the command sent to the extraocular muscles is inappropriate. Despite an abundance of supportive psychophysical investigations, the neurophysiological substrate of this process is still debated. The present study addresses this issue using H2(15)O positron emission tomography (PET). We contrasted three conditions in which healthy human subjects were required to perform saccadic eye movements toward peripheral visual targets. Two conditions involved a modification of the target location during the course of the initial saccade, when there is suppression of visual perception. In the RAND condition, intra-saccadic target displacement was random from trial-to-trial, precluding any systematic modification of the primary saccade amplitude. In the ADAPT condition, intra-saccadic target displacement was uniform, causing adaptive modification of the primary saccade amplitude. In the third condition (stationary, STAT), the target remained at the same location during the entire trial. Difference images reflecting regional cerebral-blood-flow changes attributable to the process of saccadic adaptation (ADAPT minus RAND; ADAPT minus STAT) showed a selective activation in the oculomotor cerebellar vermis (OCV; lobules VI and VII). This finding is consistent with neurophysiological studies in monkeys. Additional analyses indicated that the cerebellar activation was not related to kinematic factors, and that the absence of significant activation within the frontal eye fields (FEF) or the superior colliculus (SC) did not represent a false negative inference. Besides the contribution of the OCV to saccadic adaptation, we also observed, in the RAND condition, that the saccade amplitude was significantly larger when the previous trial involved a forward jump than when the previous trial involved a backward jump. This observation indicates that saccade accuracy is constantly monitored on a trial-to-trial basis. Behavioral measurements and PET observations (RAND minus STAT) suggest that this single-trial control of saccade amplitude may be functionally distinct from the process of saccadic adaptation.

Role of the posterior parietal cortex in updating reaching movements to a visual target.

The exact role of posterior parietal cortex (PPC) in visually directed reaching is unknown. We propose that, by building an internal representation of instantaneous hand location, PPC computes a dynamic motor error used by motor centers to correct the ongoing trajectory. With unseen right hands, five subjects pointed to visual targets that either remained stationary or moved during saccadic eye movements. Transcranial magnetic stimulation (TMS) was applied over the left PPC during target presentation. Stimulation disrupted path corrections that normally occur in response to target jumps, but had no effect on those directed at stationary targets. Furthermore, left-hand movement corrections were not blocked, ruling out visual or oculomotor effects of stimulation.

Effects of short-term adaptation of saccadic gaze amplitude on hand-pointing movements.

We investigated whether and how adaptive changes in saccadic amplitudes (short-term saccadic adaptation) modify hand movements when subjects are involved in a pointing task to visual targets without vision of the hand. An experiment consisted of the pre-adaptation test of hand pointing (placing the finger tip on a LED position), a period of adaptation, and a post-adaptation test of hand pointing. In a basic task (transfer paradigm A), the pre- and post-adaptation trials were performed without accompanying eye and head movements: in the double-step gaze adaptation task, subjects had to fixate a single, suddenly displaced visual target by moving eyes and head in a natural way. Two experimental sessions were run with the visual target jumping during the saccades, either backwards (from 30 to 20 degrees, gaze saccade shortening) or onwards (30 to 40 degrees, gaze saccade lengthening). Following gaze-shortening adaptation (level of adaptation 79+/-10%, mean and s.d.), we found a statistically significant shift (t-test, error level P<0.05) in the final hand-movement points, possibly due to adaptation transfer, representing 15.2% of the respective gaze adaptation. After gaze-lengthening adaptation (level of adaptation 92+/-17%). a non-significant shift occurred in the opposite direction to that expected from adaptation transfer. The applied computations were also performed on some data of an earlier transfer paradigm (B, three target displacements at a time) with gain shortening. They revealed a significant transfer relative to the amount of adaptation of 18.5< or = 17.5% (P<0.05). In the coupling paradigm (C), we studied the influence of gaze saccade adaptation of hand-pointing movements with concomitant orienting gaze shifts. The adaptation levels achieved were 59+/-20% (shortening) and 61+/-27% (lengthening). Shifts in the final fingertip positions were congruent with internal coupling between gaze and hand, representing 53% of the respective gaze-amplitude changes in the shortening session and 6% in the lengthening session. With an adaptation transfer of less than 20% (paradigm A and B), we concluded that saccadic adaptation does not "automatically" produce a functionally meaningful change in the skeleto-motor system controlling hand-pointing movements. In tasks with concomitant gaze saccades (coupling paradigm C), the modification of hand pointing by the adapted gaze comes out more clearly, but only in the shortening session.

From eye to hand: planning goal-directed movements.

The nature of the neural mechanisms involved in movement planning still remains widely unknown. We review in the present paper the state of our knowledge of the mechanisms whereby a visual input is transformed into a motor command. For the sake of generality, we consider the main problems that the nervous system has to solve to generate a movement, that is: target localization, definition of the initial state of the motor apparatus, and hand trajectory formation. For each of these problems three questions are addressed. First, what are the main results presented in the literature? Second, are these results compatible with each other? Third, which factors may account for the existence of incompatibilities between experimental observations or between theoritical models? This approach allows the explanation of some of the contradictions existing within the movement-generation literature. It also suggests that the search for general theories may be in vain, the central nervous system being able to use different strategies both in encoding the target location with respect to the body and in planning hand displacement. In our view, this conclusion may advance the field by both opening new lines of research and bringing some sterile controversies to an end.

Pointing errors reflect biases in the perception of the initial hand position.

By comparing the visuomotor performance of 10 adult, normal subjects in three tasks, we investigated whether errors in pointing movements reflect biased estimations of the hand starting position. In a manual pointing task with no visual feedback, subjects aimed at 48 targets spaced regularly around two starting positions. Nine subjects exhibited a similar pattern of systematic errors across targets, i.e., a parallel shift of the end points that accounted, on average, for 49% of the total variability. The direction of the shift depended on the starting location. Systematic errors decreased dramatically in the second condition where subjects were allowed to see their hand before movement onset. The third task was to use a joystick held by the left hand to estimate the location of their (unseen) right hand. The systematic perceptual errors in this condition were found to be highly correlated with the motor errors in the first condition. The results support the following conclusions. 1) Kinesthetic estimation of hand position may be consistently biased. Some of the mechanisms responsible for these biases are always active, irrespective of whether position is estimated overtly (e.g., with a matching paradigm), or covertly as part of the motor planning for aimed movements. 2) Pointing errors reflect to a significant extent the erroneous estimation of initial hand position. This suggests that aimed hand movements are planned vectorially, i.e., in terms of distance and direction, rather than in terms of absolute position in space.

A self calibration method using a soft clustering procedure for eye movement recordings.

A nearly automatic method for calibrating eye movement records has been developed. This very robust method is based on a soft clustering algorithm which allows exploration of the whole range of eye movement records for reliable calibration. In contrast to many other methods which carry out the calibration on several discrete points, this method is suitable for continuous determination of the transfer function of the eye movement transducer. Moreover it simultaneously uses the combined properties of vestibulo-ocular reflex, neck-to-eye reflex and smooth pursuit system to reach approximately a unity gain and zero phase lag (in subjects with no severe vestibular disorders or ocumomotor palsy). In addition, this method does not rely heavily on the degree of attention of the subject. The method is particularly suited for the calibration of non linear or noisy transducers like Electro Oculography (EOG). Calibration is performed within a few seconds. So when necessary in clinical applications it is possible to repeat calibrations frequently.

Final posture of the upper limb depends on the initial position of the hand during prehension movements.

The question of knowing how the nervous system transforms a desired position and orientation of the hand into a set of arm and forearm angles has been widely addressed during the last few decades. Despite this fact, it still remains unclear as to whether a unique posture of the arm is associated with every location and orientation of the hand in space. The main objective of the present study a was to address this question. To this end, we studied a prehension task requiring human subjects to reach and grasp a cylindrical object presented at different locations, along variable orientations. In contrast to previous investigations, we considered the influence of the initial position of the hand. Results showed that the posture of the arm: (1) varied systematically as a function of the movement starting point; (2) was stereotyped for a particular subject given a configuration of the object and a movement starting location; (3) was altered at both the distal and proximal levels when the orientation of the object was changed; (4) was similarly influenced by the experimental factors in all the subjects, except one. When considered together, the previous results support three main conclusions: First, the nervous system solves the joint redundancy problem using fixed strategies. Second, these fixed strategies do not provide a single correspondence between hand configuration and arm posture. Third, the position and orientation of the hand in space are unlikely to be controlled through separate independent neural pathways.

Functional anatomy of saccadic adaptation in humans.

Positron emission tomography (PET) was used to investigate the neurophysiological substrate of human saccadic adaptation. Subjects made saccadic eye movements toward a visual target that was displaced during the course of the initial saccade, a time when visual perception is suppressed. In one condition, displacement was random from trial to trial, precluding any systematic modification of the initial saccade amplitude. In the second condition, the direction and magnitude of displacement were consistent, causing adaptative modification of the initial saccade amplitude. PET difference images reflecting metabolic changes attributable to the process of saccadic adaptation showed selective activation of the medioposterior cerebellar cortex. This localization is consistent with neurophysiological findings in monkeys and brain-lesioned humans.

Viewing the hand prior to movement improves accuracy of pointing performed toward the unseen contralateral hand.

It is now well established that the accuracy of pointing movements to visual targets is worse in the full open loop condition (FOL; the hand is never visible) than in the static closed loop condition (SCL; the hand is only visible in static position prior to movement onset). In order to account for this result, it is generally admitted that viewing the hand in static position (SCL) improves the movement planning process by allowing a better encoding of the initial state of the motor apparatus. Interestingly, this wide-spread interpretation has recently been challenged by several studies suggesting that the effect of viewing the upper limb at rest might be explained in terms of the simultaneous vision of the hand and target. This result is supported by recent studies showing that goal-directed movements involve different types of planning (egocentric versus allocentric) depending on whether the hand and target are seen simultaneously or not before movement onset. The main aim of the present study was to test whether or not the accuracy improvement observed when the hand is visible before movement onset is related, at least partially, to a better encoding of the initial state of the upper limb. To address this question, we studied experimental conditions in which subjects were instructed to point with their right index finger toward their unseen left index finger. In that situation (proprioceptive pointing), the hand and target are never visible simultaneously and an improvement of movement accuracy in SCL, with respect to FOL, may only be explained by a better encoding of the initial state of the moving limb when vision is present. The results of this experiment showed that both the systematic and the variable errors were significantly lower in the SCL than in the FOL condition. This suggests: (1) that the effect of viewing the static hand prior to motion does not only depend on the simultaneous vision of the goal and the effector during movement planning; (2) that knowledge of the initial upper limb configuration or position is necessary to accurately plan goal-directed movements; (3) that static proprioceptive receptors are partially ineffective in providing an accurate estimate of the limb posture, and/or hand location relative to the body; and (4) that static visual information significantly improves the representation provided by the static proprioceptive channel.

Constrained and unconstrained movements involve different control strategies.

This experiment was carried out to test whether or not the rules governing the execution of compliant and unconstrained movements are different (a compliant motion is defined as a motion constrained by external contact). To answer this question we examined the characteristics of visually directed movements performed with either the index fingertip (unconstrained) or a hand-held cursor (compliant). For each of these categories of movements, two experimental conditions were investigated: no instruction about hand path, and instruction to move the fingertip along a straight-line path. The results of the experiment were as follows: 1) The spatiotemporal characteristics of the compliant and unconstrained movements were fundamentally different when the subjects were not required to follow a specific hand path. 2) The instruction to perform straight movements modified the characteristics of the unconstrained movements, but not those of the compliant movements. 3) The target eccentricity influenced selectively the curvature of the "unconstrained-no path instruction" movements. Taken together, these results suggest that compliant and unconstrained movements involve different control strategies. Our data support the hypothesis that unconstrained motions are, unlike compliant motions, not programmed to follow a straight-line path in the task space. These observations provide a theoretical reference frame within which some apparently contradictory results reported in the movement generation literature may be explained.

Postural control of three-dimensional prehension movements.

This experiment was carried out to test the hypothesis that three-dimensional upper limb movements could be initiated and controlled in the joint space via a mechanism comparing an estimate of the current postural state of the upper arm with a target value determined by one specific inverse static transform converting the coordinates of the object into a set of arm, forearm, and wrist angles. This hypothesis involves two main predictions: 1) despite joint redundancy, the posture reached by the upper limb should be invariant for a given context; and 2) a movement programmed in joint space should exhibit invariant characteristics of the joint covariation pattern as well as a corresponding variable hand path curvature in the task space. To test these predictions, we examined prehension movements toward a cylindrical object presented at a fixed spatial location and at various orientations without vision of the moving limb. Once presented, the object orientation was either kept constant (unperturbed trials) or suddenly modified at movement onset (perturbed trials). Three-dimensional movement trajectories were analyzed in both joint and task spaces. For the unperturbed trials, the task space analysis showed a variable hand path curvature depending on object orientation. The joint space analysis showed that the seven final angles characterizing the upper limb posture at hand-to-object contact varied monotonically with object orientation. At a dynamic level, movement onset and end were nearly identical for all joints. Moreover, for all joints having a monotonic variation, maximum velocity occurred almost simultaneously. For the elbow, the only joint presenting a reversal, the reversal was synchronized with the time to peak velocity of the other joint angles. For the perturbed trials, a smooth and complete compensation of the movement trajectory was observed in the task space. At a static level the upper limb final posture was identical to that obtained when the object was initially presented at the orientation following the perturbation. This result was particularly remarkable considering the large set of comfortable postures allowed by joint redundancy. At a dynamic level, the joints' covariation pattern was updated to reach the new target posture. The initial synergies were not disrupted by the perturbation, but smoothly modified, the different joints' movements ending nearly at the same time. Taken together, these results support the hypothesis that prehension movements are initiated and controlled in the joint space on the basis of a joint angular error vector rather than a spatial error vector.

On the short-term adaptation of eye saccades and its transfer to head movements.

During a sequence of eye saccades toward a target that is systematically displaced during initiation of the saccade, the oculomotor system adjusts saccadic amplitude and direction in less than 100 trials to directly reach the second target position. The goal of the present work was to test whether and under which conditions these short-term, adaptive modifications in eye movements are transferred from horizontal eye saccades to horizontal head-pointing movements. In the first series of experiments subjects had to execute head yaw rotations to an extent defined by verbal command (assessed movements). These head movements were not part of visually elicited gaze shifts. They were recorded before and after a period of saccadic adaptation. Saccades were adapted to reduced amplitudes by using target displacements from 30 to 20 degrees and from 40 to 30 degrees. After 40-50 trials per target displacement, the amount of eye saccade adaptation was 79% (30-20 degrees) and 97% (40-30 degrees) of the displacement amplitude. In the second series of experiments, visually triggered head movements to briefly illuminated targets (100 ms) were measured before and after adaptation. The data obtained from both series did not reveal a functionally significant transfer of saccadic adaptation to head movements. The amount of possible transfer given as a percentage of the amount of achieved adaptation was: assessed head movements, 40 degrees, 1.9%, 20 degrees, -8.6%; visually triggered movements, 40 degrees, 5.1%, 20 degrees, 10.0%. No values significantly deviated from zero.

Pointing movement in an artificial perturbing inertial field: a prospective paradigm for motor control study.

The present experiment focused on spatial accuracy and kinematics of fast pointing movements submitted to a multi-directional inertial perturbation. Pointing movements were performed without direct visual control, on a rotating armchair adding centrifugal and Coriolis forces to the natural displacement of the arm. The simultaneous action of these two forces induced a perturbation of the arm displacement both in amplitude and direction. Results showed that these two parameters were adjusted differently according to their own temporal constraint. Movement amplitude was adjusted on-line from the very first trial through the amendment of the whole acceleration pattern. Conversely, adjustment to directional perturbation was progressively achieved through several movement rehearsals. This correction appeared to be primarily due to a modification of the initial orientation of the arm trajectory, based seemingly on kinaesthetic knowledge from previous performances. The amendment of spatial parameters during motor response in the perturbing environment was discussed with an emphasis on the involvement of the cerebellum in reaching movement and the learning process.

Integrated control of hand transport and orientation during prehension movements.

At a descriptive level, prehension movements can be partitioned into three components ensuring, respectively, the transport of the arm to the vicinity of the target, the orientation of the hand according to object tilt, and the grasp itself. Several authors have suggested that this analytic description may be an operational principle for the organization of the motor system. This hypothesis, called "visuomotor channels hypothesis," is in particular supported by experiments showing a parallelism between the reach and grasp components of prehension movements. The purpose of the present study was to determine whether or not the generalization of the visuomotor channels hypothesis, from its initial form, restricted to the grasp and transport components, to its actual form, including the reach orientation and grasp components, may be well founded. Six subjects were required to reach and grasp cylindrical objects presented at a given location, with different orientations. During the movements, object orientation was either kept constant (unperturbed trials) or modified at movement onset (perturbed trials). Results showed that both wrist path (sequence of positions that the hand follows in space), and wrist trajectory (time sequence of the successive positions of the hand) were strongly affected by object orientation and by the occurrence of perturbations. These observations suggested strongly that arm transport and hand orientation were neither planned nor controlled independently. The significant linear regressions observed, with respect to the time, between arm displacement (integral of the magnitude of the velocity vector) and forearm rotation also supported this view. Interestingly, hand orientation was not implemented at only the distal level, demonstrating that all the redundant degrees of freedom available were used by the motor system to achieve the task. The final configuration reached by the arm was very stable for a given final orientation of the object to grasp. In particular, when object tilt was suddenly modified at movement onset, the correction brought the upper limb into the same posture as that obtained when the object was initially presented along the final orientation reached after perturbation. Taken together, the results described in the present study suggest that arm transport and hand orientation do not constitute independent visuomotor channels. They also further suggest that prehension movements are programmed, from an initial configuration, to reach smoothly a final posture that corresponds to a given "location and orientation" as a whole.

Modifications in end positions of arm movements following short-term saccadic adaptation.

We investigated whether short-term saccadic adaptation modifies hand pointing. Subjects were presented with double-step targets, the second target jump occurring during the saccade to the first one and bringing the target back to 66% of the first target eccentricity, in order to reduce the gain of their gaze saccades. Before and after this adaptation phase, they pointed with their hand to single step targets while keeping their gaze straight ahead. The results show that the hand movements terminated at positions that were significantly less eccentric following the adaptation phase, resembling the adaptive modification seen in the gaze movements. These results suggest that the motor systems controlling gaze and hand use common information about target position.