Saccade adaptation improves in response to a gradually introduced stimulus perturbation

A major goal in the study of motor learning is to improve the extent to which subjects adapt their movements in response to errors. Recent attention has focused on the gradual-adaptation paradigm, in which an adaptive stimulus is introduced incrementally, rather than all at once as in conventional adaptation paradigms. However, there is disagreement - even among studies involving the same sensorimotor-learning task - as to the robustness of this approach. In particular, although all studies confirm that retention of learning is improved, not all agree that exposure to a gradual-adaptation paradigm can improve the extent of adaptation that takes place. Also, the paradigm has not previously been studied with saccadic eye movements, which are unique in that they typically lack online error feedback during each movement. To determine the effectiveness of gradual adaptation in this system, we compared saccadic adaptation performed with gradual and conventional adaptation paradigms. We find evidence consistent with more robust adaptation - in the sense of greater extent of adaptation as well as greater retention of learning (larger aftereffects) - in response to a gradual adaptation stimulus. The results suggest the need to develop alternative models of motor learning, as current error-based modeling efforts are unable to account for the increased extent of adaptation when subjects are only exposed to the full adaptive stimulus for a brief time.     

Functional significance of stiffness in adaptation of multijoint arm movements to stable and unstable dynamics

This study compared the mechanisms of adaptation to stable and unstable dynamics from the perspective of changes in joint mechanics. Subjects were instructed to make point to point movements in force fields generated by a robotic manipulandum which interacted with the arm in either a stable or an unstable manner. After subjects adjusted to the initial disturbing effects of the force fields they were able to produce normal straight movements to the target. In the case of the stable interaction, subjects modified the joint torques in order to appropriately compensate for the force field. No change in joint torque or endpoint force was required or observed in the case of the unstable interaction. After adaptation, the endpoint stiffness of the arm was measured by applying displacements to the hand in eight different directions midway through the movements. This was compared to the stiffness measured similarly during movements in a null force field. After adaptation, the endpoint stiffness under both the stable and unstable dynamics was modified relative to the null field. Adaptation to unstable dynamics was achieved by selective modification of endpoint stiffness in the direction of the instability. To investigate whether the change in endpoint stiffness could be accounted for by change in joint torque or endpoint force, we estimated the change in stiffness on each trial based on the change in joint torque relative to the null field. For stable dynamics the change in endpoint stiffness was accurately predicted. However, for unstable dynamics the change in endpoint stiffness could not be reproduced. In fact, the predicted endpoint stiffness was similar to that in the null force field. Thus, the change in endpoint stiffness seen after adaptation to stable dynamics was directly related to changes in net joint torque necessary to compensate for the dynamics in contrast to adaptation to unstable dynamics, where a selective change in endpoint stiffness occurred without any modification of net joint torque.     

Saccade adaptation as a model of learning in voluntary movements

Motor learning ensures the accuracy of our daily movements. However, we know relatively little about its mechanisms, particularly for voluntary movements. Saccadic eye movements serve to bring the image of a visual target precisely onto the fovea. Their accuracy is maintained not by on-line sensory feedback but by a learning mechanism, called saccade adaptation. Recent studies on saccade adaptation have provided valuable additions to our knowledge of motor learning. This review summarizes what we know about the characteristics and neural mechanisms of saccade adaptation, emphasizing recent findings and new ideas. Long-term adaptation, distinct from its short-term counterpart, seems to be present in the saccadic system. Accumulating evidence indicates the involvement of the oculomotor cerebellar vermis as a learning site. The superior colliculus is now suggested not only to generate saccade commands but also to issue driving signals for motor learning. These and other significant contributions have advanced our understanding of saccade adaptation and motor learning in general.     

Development of postural adaptation to arm raising

We studied the development of the coordination between posture and movement by analyzing the shifts of the center of pressure (CoP) associated with arm raising. Three groups of children aged 3–5 years, 6–8 years, and 9–10 years and an adult group were tested. The subjects were required to raise their arms to the horizontal position while standing still, with their hands free or loaded (5% of the body weight). The arm movements were recorded by a TV-image processor, and the changes in position of the CoP were measured by a force platform and analyzed before, during, and after the arm movement. The data show that the CoP moved forward during arm raising, that additional load induced a greater shift in all age groups, and that the relative amplitude of the shift decreased with age. The greatest changes occurred between ages 3–5 years and 6–8 years. The pre- and postmovement CoP shift suggests qualitative changes in the postural adaptation to movement between these two age groups: the anticipatory postural adjustments moved from a supporting function to a compensatory function, yielding an increasing functional convergence between the feedforward and the feedback modes of postural control, and an increasing rapidness in recovering postural stability after arm movement. The postural behavior shown by the 9- to 10-year-old children and by the adults in the arms-free condition suggests an increased tolerance to unbalance when postural oscillations do not jeopardize static equilibrium. Electronic Publication     

Threshold control of arm posture and movement adaptation to load

We addressed the fundamental questions of which variables underlie the control of arm movement and how they are stored in motor memory, reproduced and modified in the process of adaptation to changing load conditions. Such variables are defined differently in two major theories of motor control (internal models and threshold control). To resolve the controversy, these theories were tested (experiment 1) based on their ability to explain why active movement away from a stable posture is not opposed by stabilizing mechanisms (the posture–movement problem). The internal model theory suggests that the system counteracts the opposing forces by increasing the muscle activity in proportion to the distance from the initial posture (position-dependent EMG control). In contrast, threshold control fully excludes these opposing forces by shifting muscle activation thresholds and thus resetting the stabilizing mechanisms to a new posture. Subjects were sitting, holding the vertical handle of a double-joint manipulandum with their right hand and were facing a computer screen on which the handle and target to be reached were displayed. In response to an auditory signal, subjects quickly moved the handle from an initial position to one of two (frontal and sagittal) targets. No load was applied during the movement but in separate trials, a brief perturbation was applied to the handle by torque motors controlling the manipulandum. Perturbations were applied prior to or 3 s after movement offset, in the latter case in one of eight directions. The EMG activity of the majority of the seven recorded muscles was at zero level before movement onset and returned to zero level after movement offset. Those muscles that remained active before or after the movement could be made silent whereas previously silent muscles could be activated after a small passive displacement (several millimeters) elicited by perturbations in appropriate directions. Results showed that the activation thresholds of motoneurons of arm muscles were reset from the initial to a final position and that EMG activity was not position-dependent. These results were inconsistent with the internal model theory but confirmed the threshold control theory. Then the ability of threshold control theory to explain rapid movement adaptation to a position-dependent load was investigated (experiment 2 and 3). Subjects produced fast movement to the frontal target with and without a position-dependent load applied to the handle. Trials were organized in blocks alternating between the load and no-load condition (20 blocks in total, with randomly chosen number of five to ten trials in each). Subjects were instructed “do not correct” in experiment 2 and “correct” movement errors during the trial in experiment 3. Five threshold arm configurations underlying the movement production and adaptation were identified. When instructed “do not correct”, movement precision was fully restored on average after two trials. No significant improvement was observed as the experiment progressed despite the fact that the same load condition was repeated after one block of trials. Thus, in each block, the adaptation was made anew, implying that subjects relied on short-term memory and could not recall the threshold arm configurations they specified to accurately reach the same target in the same load condition in previous blocks. When instructed to “correct” within each trial, precision was restored faster, on average after one trial. Major aspects of the production and adaptation of arm movement (including the kinematics, movement errors, instruction-dependent behavior, and absence of position-related EMG activity) are explained in terms of threshold control.     

Contributions of altered stretch reflex coordination to arm impairments following stroke

Patterns of stereotyped muscle coactivation, clinically referred to as synergies, emerge following stroke and impair arm function. Although researchers have focused on cortical contributions, there is growing evidence that altered stretch reflex pathways may also contribute to impairment. However, most previous reflex studies have focused on passive, single-joint movements without regard to their coordination during volitional actions. The purpose of this study was to examine the effects of stroke on coordinated activity of stretch reflexes elicited in multiple arm muscles following multijoint perturbations. We hypothesized that cortical injury results in increased stretch reflexes of muscles characteristic of the abnormal flexor synergy during active arm conditions. To test this hypothesis, we used a robot to apply position perturbations to impaired arms of 10 stroke survivors and dominant arms of 8 healthy age-matched controls. Corresponding reflexes were assessed during volitional contractions simulating different levels of gravitational support, as well as during voluntary flexion and extension of the elbow and shoulder. Reflexes were quantified by average rectified surface electromyogram, recorded from eight muscles spanning the elbow and shoulder. Reflex coordination was quantified using an independent components analysis. We found stretch reflexes elicited in the stroke group were significantly less sensitive to changes in background muscle activation compared with those in the control group (P < 0.05). We also observed significantly increased reflex coupling between elbow flexor and shoulder abductor-extensor muscles in stroke subjects relative to that in control subjects. This increased coupling was present only during volitional tasks that required elbow flexion (P < 0.001), shoulder extension (P < 0.01), and gravity opposition (P < 0.01), but not during the "no load" condition. During volitional contractions, reflex amplitudes scaled with the level of impairment, as assessed by Fugl-Meyer scores (r(2) = 0.63; P < 0.05). We conclude that altered reflex coordination is indicative of motor impairment level and may contribute to impaired arm function following stroke.     

Sensorimotor adaptation in response to proprioceptive bias

Studies investigating visuo-motor adaptation typically introduce sensory conflicts by manipulating visual information (prisms, cursor gains). The purpose of the present study was to determine whether similar adaptation would be observed when a conflict is created through distortion of the proprioceptive sense, rather than through visual distortion. We used a coordinated movement task that required participants to release thumb and index finger at a specific elbow angle during passive elbow extension. Participants could not see their arm, but were shown a cursor representing the forearm on a video screen. In the proprioceptive group, a sensory conflict was introduced by vibrating the biceps brachii muscle, introducing a discrepancy of approximately 7.5° between the proprioceptively perceived and visually perceived elbow angle. In the visual group, a conflict of similar magnitude was obtained by introducing a gain of 7.5° to the cursor with respect to forearm position. Adaptation was assessed by the presence of plastic changes in release elbow angles following a period of exposure to the sensory conflict (i.e., aftereffects). Both groups showed high accuracy during exposure despite the sensory conflicts. More importantly, the visual group presented large and persistent aftereffects, while the proprioceptive group presented none. We suggest that the proprioceptive group’s lack of adaptation was due to the artificial muscle spindle activity resulting from vibration, which prevented visual and proprioceptive signals to be merged into a common frame of reference.     

Osteoblast response to biomimetically altered titanium surfaces

Bioinert titanium (Ti) materials are generally encapsulated by fibrous tissue after implantation into the living body. To improve the bone-bonding ability of Ti implants, we activated commercially pure titanium (cpTi) by a simple chemical pre-treatment in HCl and NaOH. Subsequently, we exposed the treated samples to simulated body fluid (SBF) for 2 (TiCT) and 14 days (TiHCA), respectively, to mimic the early stages of bone bonding and to investigate the in vitro response of osteoblasts on thus altered biomimetic surfaces. Sample surfaces were characterized by scanning electron microscopy, energy-dispersive X-ray analysis, cross-sectional transmission electron microscopy analyses, Fourier transform infrared and Raman spectroscopy. It was shown that the efflorescence consisting of sodium titanate that is present on pre-treated cpTi surfaces transformed to calcium titanate after 2 days in SBF. After 14 days in SBF a homogeneous biomimetic apatite layer precipitated. Human osteoblasts (MG-63) revealed a well spread morphology on both functionalized Ti surfaces. On TiCT, the gene expression of the differentiation proteins alkaline phosphatase (ALP) and bone sialo protein was increased after 2 days. On both TiCT and TiHCA, the collagen I and ALP expression on the protein level was enhanced at 7 and 14 days. The TiCT and the TiHCA surfaces reveal the tendency to increase the differentiated cell function of MG-63 osteoblasts. Thus, chemical pre-treatment of titanium seems to be a promising method to generate osteoconductive surfaces.     

Inter-joint coupling strategy during adaptation to novel viscous loads in human arm movement

When arm movements are perturbed by a load, how does the nervous system adjust control signals to reduce error? While it has been shown that the nervous system is capable of compensating for the effects of limb dynamics and external forces, the strategies used to adapt to novel loads are not well understood. We used a robotic exoskeleton [kinesiological instrument for normal and altered reaching movements (KINARM)] to apply novel loads to the arm during single-joint elbow flexions in the horizontal plane (shoulder rotation was allowed). Loads varied in magnitude with the instantaneous velocity of elbow flexion, and were applied to the shoulder in experiment 1 (interaction loads) and the elbow in experiment 2 (direct loads). Initial exposure to both interaction and direct loads resulted in perturbations at both joints, even though the load was applied to only a single joint. Subjects tended to correct for the kinematics of the elbow joint while perturbations at the shoulder persisted. Electromyograms (EMGs) and computed muscle torque showed that subjects modified muscle activity at the elbow to reduce elbow positional deviations. Shoulder muscle activity was also modified; however, these changes were always in the same direction as those at the elbow. Current models of motor control based on inverse-dynamics calculations and force-control, as well as models based on positional control, predict an uncoupling of shoulder and elbow muscle torques for adaptation to these loads. In contrast, subjects in this study adopted a simple strategy of modulating the natural coupling that exists between elbow and shoulder muscle torque during single-joint elbow movements.     

Central programming of postural movements: adaptation to altered support-surface configurations

We studied the extent to which automatic postural actions in standing human subjects are organized by a limited repertoire of central motor programs. Subjects stood on support surfaces of various lengths, which forced them to adopt different postural movement strategies to compensate for the same external perturbations. We assessed whether a continuum or a limited set of muscle activation patterns was used to produce different movement patterns and the extent to which movement patterns were influenced by prior experience. Exposing subjects standing on a normal support surface to brief forward and backward horizontal surface perturbations elicited relatively stereotyped patterns of leg and trunk muscle activation with 73- to 110-ms latencies. Activity began in the ankle joint muscles and then radiated in sequence to thigh and then trunk muscles on the same dorsal or ventral aspect of the body. This activation pattern exerted compensatory torques about the ankle joints, which restored equilibrium by moving the body center of mass forward or backward. This pattern has been termed the ankle strategy because it restores equilibrium by moving the body primarily around the ankle joints. To successfully maintain balance while standing on a support surface short in relation to foot length, subjects activated leg and trunk muscles at similar latencies but organized the activity differently. The trunk and thigh muscles antagonistic to those used in the ankle strategy were activated in the opposite proximal-to-distal sequence, whereas the ankle muscles were generally unresponsive. This activation pattern produced a compensatory horizontal shear force against the support surface but little, if any, ankle torque. This pattern has been termed the hip strategy, because the resulting motion is focused primarily about the hip joints. Exposing subjects to horizontal surface perturbations while standing on support surfaces intermediate in length between the shortest and longest elicited more complex postural movements and associated muscle activation patterns that resembled ankle and hip strategies combined in different temporal relations. These complex postural movements were executed with combinations of torque and horizontal shear forces and motions of ankle and hip joints. During the first 5-20 practice trials immediately following changes from one support surface length to another, response latencies were unchanged. The activation patterns, however, were complex and resembled the patterns observed during well-practiced stance on surfaces of intermediate lengths.(ABSTRACT TRUNCATED AT 400 WORDS)     

Different mechanisms involved in adaptation to stable and unstable dynamics

Recently, we demonstrated that humans can learn to make accurate movements in an unstable environment by controlling magnitude, shape, and orientation of the endpoint impedance. Although previous studies of human motor learning suggest that the brain acquires an inverse dynamics model of the novel environment, it is not known whether this control mechanism is operative in unstable environments. We compared learning of multijoint arm movements in a "velocity-dependent force field" (VF), which interacted with the arm in a stable manner, and learning in a "divergent force field" (DF), where the interaction was unstable. The characteristics of error evolution were markedly different in the 2 fields. The direction of trajectory error in the DF alternated to the left and right during the early stage of learning; that is, signed error was inconsistent from movement to movement and could not have guided learning of an inverse dynamics model. This contrasted sharply with trajectory error in the VF, which was initially biased and decayed in a manner that was consistent with rapid feedback error learning. EMG recorded before and after learning in the DF and VF are also consistent with different learning and control mechanisms for adapting to stable and unstable dynamics, that is, inverse dynamics model formation and impedance control. We also investigated adaptation to a rotated DF to examine the interplay between inverse dynamics model formation and impedance control. Our results suggest that an inverse dynamics model can function in parallel with an impedance controller to compensate for consistent perturbing force in unstable environments.     

Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads.

The biophysical mechanisms that drive and regulate cardiac looping are not well understood, but mechanical forces likely play a central role. Previous studies have shown that cardiac torsion, which defines left-right directionality, is caused largely by forces exerted on the heart tube by a membrane called the splanchnopleure (SPL). Here we show that, when the SPL is removed from the embryonic chick heart, torsion is initially suppressed. Several hours later, however, normal torsion is restored. This delayed torsion coincides with increased myocardial stiffness, especially on the right side of the heart. Exposure to the myosin inhibitor Y-27632 suppressed both responses, suggesting that the delayed torsion is caused by an abnormal cytoskeletal contraction. This hypothesis is supported further by computational modeling. These results suggest that the looping embryonic heart has the ability to adapt to changes in the mechanical environment, which may play a regulatory role during morphogenesis.     

Proprioceptive illusions created by vibration of one arm are altered by vibrating the other arm

There is some evidence that signals coming from both arms are used to determine the perceived position and movement of one arm. We examined whether the sense of position and movement of one (reference) arm is altered by increases in muscle spindle signals in the other (indicator) arm in blindfolded participants (n = 26). To increase muscle spindle discharge, we applied 70–80 Hz muscle vibration to the elbow flexors of the indicator arm. In a first experiment, proprioceptive illusions in the vibrated reference arm in a forearm position-matching task were compared between conditions in which the indicator arm elbow flexors were vibrated or not vibrated. We found that the vibration illusion of arm extension induced by vibration of reference arm elbow flexors was reduced in the presence of vibration of the indicator elbow flexors. In a second experiment, participants were asked to describe their perception of the illusion of forearm extension movements of the reference arm evoked by vibration of reference arm elbow flexors in response to on/off and off/on transitions of vibration of non-reference arm elbow flexors. When vibration of non-reference arm elbow flexors was turned on, they reported a sensation of slowing down of the illusion of the reference arm. When it was turned off, they reported a sensation of speeding up. To conclude, the present study shows that both the sense of limb position and the sense of limb movement of one arm are dependent to some extent on spindle signals coming from the other arm.     

The inflammatory response to vaccination is altered in the elderly

To further explore whether immune function and acute phase response are altered during ageing, the response to a mild inflammatory stress (DT-Polio-Typhim vaccination) was studied in elderly and young subjects. Cytokine production (IFN-gamma, TNF-alpha, IL-6, IL-10) by whole blood cultures, circulating cytokines and acute phase proteins were analysed before and 2 days after vaccination. Prior to vaccination, only IFN-gamma production was lower in the elderly than in the young subjects due to a lower mononuclear cell number. In the same time, although in the normal range, several acute phase proteins were greater in elderly than in young subjects, suggesting a low-grade inflammatory state in the elderly. After vaccination, IFN-gamma production remained lower in the elderly than in the young, supporting an altered cell-mediated immunity with advancing age. TNF-alpha production was unaffected by either ageing or vaccination. IL-6 production was stimulated by vaccination in young subjects but not significantly in the elderly. IL-10 production was inhibited by vaccination in the elderly but not in the young. Acute phase proteins were less increased in elderly than in young subjects. Taken together, these results support a general lack of inflammatory response in the elderly exposed to an immune challenge and suggest that immune deficiency may concern both Th1 and Th2 responses. However, the interpretation must respect the limitation of small subjects number.     

Saccade generation and suppression in schizophrenia: effects of response switching and perseveration

Poor antisaccade performance is a reliable index of action control deficits in schizophrenia. To further elucidate the underlying cognitive impairments, the current study aimed to confirm effects of switching the response direction on saccadic performance and to investigate whether response switch effects relate to perseveration. Fourteen schizophrenia patients and 14 healthy controls performed sequences of 1 to 3 simple volitional saccades to one direction and a subsequent volitional saccade with distractor to the same or the opposite direction. Response switches increased error rates in schizophrenia if they followed 3 saccades to the opposite side, suggesting that response switching affects performance on conditions of strong persisting response programs. The increase of response switch error rates with multiple repetitions of the prior response points to a relationship between perseveration and response selection.     

Learned dynamics of reaching movements generalize from dominant to nondominant arm

Accurate performance of reaching movements depends on adaptable neural circuitry that learns to predict forces and compensate for limb dynamics. In earlier experiments, we quantified generalization from training at one arm position to another position. The generalization patterns suggested that neural elements learning to predict forces coded a limb's state in an intrinsic, muscle-like coordinate system. Here, we test the sensitivity of these elements to the other arm by quantifying inter-arm generalization. We considered two possible coordinate systems: an intrinsic (joint) representation should generalize with mirror symmetry reflecting the joint's symmetry and an extrinsic representation should preserve the task's structure in extrinsic coordinates. Both coordinate systems of generalization were compared with a na?ve control group. We tested transfer in right-handed subjects both from dominant to nondominant arm (D-->ND) and vice versa (ND-->D). This led to a 2 x 3 experimental design matrix: transfer direction (D-->ND/ND-->D) by coordinate system (extrinsic, intrinsic, control). Generalization occurred only from dominant to nondominant arm and only in extrinsic coordinates. To assess the dependence of generalization on callosal inter-hemispheric communication, we tested commissurotomy patient JW. JW showed generalization from dominant to nondominant arm in extrinsic coordinates. The results suggest that when the dominant right arm is used in learning dynamics, the information could be represented in the left hemisphere with neural elements tuned to both the right arm and the left arm. In contrast, learning with the nondominant arm seems to rely on the elements in the nondominant hemisphere tuned only to movements of that arm.     

Restrained eaters show altered brain response to food odor

Do restrained and unrestrained eaters differ in their brain response to food odor? We addressed this question by examining restrained eaters' brain response to food (chocolate) and non-food (geraniol, floral) odors, both when odor was attended to and when ignored. Using olfactory event-related potentials (OERPs), we found that restrained eaters and controls responded similarly to the non-food odor; however, unlike controls, restrained eaters showed no increase in brain response to the food odor when they focused attention on it. Rather, restrained eaters showed attenuated OERP amplitudes to the food odor in both attended and ignored conditions, suggesting that the brain's response to attended food odor was abnormally suppressed.