The relative contribution of retinal and extraretinal signals in determining the accuracy of reaching movements in normal subjects and a deafferented patient

This experiment investigated the relative extent to which different signals from the visuo-oculomotor system are used to improve accuracy of arm movements. Different visuo-oculomotor conditions were used to produce various retinal and extraretinal signals leading to a similar target amplitude: (a) fixating a central target while pointing to a peripheral visual target, (b) tracking a target through smooth pursuit movement and then pointing to the target when its excursion ceased, and (c) pointing to a target reached previously by a saccadic eye movement. The experiment was performed with a deafferented subject and control subjects. For the deafferented patient, the absence of proprioception prevented any comparison between internal representations of target and limb (through proprioception) positions during the arm movement. The deafferented patient's endpoint therefore provided a good estimate of the accuracy of the target coordinates used by the arm motor system. The deafferented subject showed relatively good accuracy by producing a saccade prior to the pointing, but large overshooting in the fixation condition and undershooting in the pursuit condition. The results suggest that the deafferented subject does use oculomotor signals to program arm movement and that signals associated with fast movements of the eyes are better for pointing accuracy than slow ramp movements. The inaccuracy of the deafferented subject when no eye movement is allowed (the condition in which the controls were the most accurate) suggests that, in this condition, a proprioceptive map is involved in which both the target and the arm are represented.     

The effect of neonatal deafferentation or deefferentation on the immunocytochemistry of muscle spindles in the rat

Immature muscle spindles were either deafferented or deefferented by selectively severing the sensory or motor nerve supply to the soleus muscle in neonatal rats. Experimental spindles were examined two months after the surgery using monoclonal antibodies specific for myosin heavy chains of slow-tonic and fast-twitch chicken muscles. The deefferented spindles exhibited a pattern of antibody binding that closely resembled that of normal adult intrafusal fibers, whereas deafferented intrafusal fibers were unreactive with the two antibodies. These observations suggest that sensory innervation is responsible for the expression of myosins in developing intrafusal muscle fibers of rat.     

Arm–trunk coordination in the absence of proprioception

During trunk-assisted reaching to targets placed within arms length, the influence of trunk motion on the hand trajectory is compensated for by changes in the arm configuration. The role of proprioception in this compensation was investigated by analyzing the movements of 2 deafferented and 12 healthy subjects. Subjects reached to remembered targets (placed ~80° ipsilateral or ~45° contralateral to the sagittal midline) with an active forward movement of the trunk produced by hip flexion. In 40% of randomly selected trials, trunk motion was mechanically blocked. No visual feedback was provided during the experiment. The hand trajectory and velocity profiles of healthy subjects remained invariant whether or not the trunk was blocked. The invariance was achieved by changes in arm interjoint coordination that, for reaches toward the ipsilateral target, started as early as 50 ms after the perturbation. Both deafferented subjects exhibited considerable, though incomplete, compensation for the effects of the perturbation. Compensation was more successful for reaches to the ipsilateral target. Both deafferented subjects showed invariance between conditions (unobstructed or blocked trunk motion) in their hand paths to the ipsilateral target, and one did to the contralateral target. For the other deafferented subject, hand paths in the two types of trials began to deviate after about 50% into the movement, because of excessive elbow extension. In movements to the ipsilateral target, when deafferented subjects compensated successfully, the changes in arm joint angles were initiated as early as 50 ms after the trunk perturbation, similar to healthy subjects. Although the deafferented subjects showed less than ideal compensatory control, they compensated to a remarkably large extent given their complete loss of proprioception. The presence of partial compensation in the absence of vision and proprioception points to the likelihood that not only proprioception but also vestibulospinal pathways help mediate this compensation.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Bimanual coordination during rhythmic movements in the absence of somatosensory feedback

We investigated the role of somatosensory feedback during bimanual coordination by testing a bilaterally deafferented patient, a unilaterally deafferented patient, and three control participants on a repetitive bimanual circle-drawing task. Circles were drawn symmetrically or asymmetrically at varying speeds with full, partial, or no vision of the hands. Strong temporal coupling was observed between the hands at all movement rates during symmetrical drawing and at the comfortable movement rate during asymmetrical drawing in all participants. When making asymmetric movements at the comfortable and faster rates, the patients and controls exhibited similar evidence of pattern instability, including a reduction in temporal coupling and trajectory deformation. The patients differed from controls on measures of spatial coupling and variability. The amplitudes and shapes of the two circles were less similar across limbs for the patients than the controls and the circles produced by the patients tended to drift in extrinsic space across successive cycles. These results indicate that somatosensory feedback is not critical for achieving temporal coupling between the hands nor does it contribute significantly to the disruption of asymmetrical coordination at faster movement rates. However, spatial consistency and position, both within and between limbs, were disrupted in the absence of somatosensory feedback.     

Reference systems for coding spatial information in normal subjects and a deafferented patient

To produce accurate goal-directed arm movements, subjects must determine the precise location of target object. Position of extracorporeal objects can be determined using: (a) an egocentric frame of reference, in which the target is localized in relation to the position of the body; and/or (b) an allocentric system, in which target position is determined in relation to stable visual landmarks surrounding the target (Bridgeman 1989; Paillard 1991). The present experiment was based on the premise that (a) the presence of a structured visual environment enables the use of an allocentric frame of reference, and (b) the sole presence of a visual target within a homogeneous background forces the registration of the target location by an egocentric system. Normal subjects and a deafferented patient (i.e., with an impaired egocentric system) pointed to visual targets presented in both visual environments to evaluate the efficiency of the two reference systems. For normals, the visual environment conditions did not affect pointing accuracy. However, kinematic parameters were affected by the presence or absence of a structured visual surrounding. For the deafferented patient, the presence of a structured visual environment permitted a decrease in spatial errors when compared with the unstructured surrounding condition (for movements with or without visual feedback of the trajectory). Overall, results support the existence of an egocentric and an allocentric reference system capable of organizing extracorporeal space during arm movements directed toward visual targets.     

Variant and invariant features characterizing natural and reverse whole-body pointing movements

Our previous studies of interlimb asymmetries during reaching movements have given rise to the dynamic-dominance hypothesis of motor lateralization. This hypothesis proposes that dominant arm control has become optimized for efficient intersegmental coordination, which is often associated with straight and smooth hand-paths, while non-dominant arm control has become optimized for controlling steady-state posture, which has been associated with greater final position accuracy when movements are mechanically perturbed, and often during movements made in the absence of visual feedback. The basis for this model of motor lateralization was derived from studies conducted in right-handed subjects. We now ask whether left-handers show similar proficiencies in coordinating reaching movements. We recruited right- and left-handers (20 per group) to perform reaching movements to three targets, in which intersegmental coordination requirements varied systematically. Our results showed that the dominant arm of both left- and right-handers were well coordinated, as reflected by fairly straight hand-paths and low errors in initial direction. Consistent with our previous studies, the non-dominant arm of right-handers showed substantially greater curvature and large errors in initial direction, most notably to targets that elicited higher intersegmental interactions. While the right, non-dominant, hand-paths of left-handers were slightly more curved than those of the dominant arm, they were also substantially more accurate and better coordinated than the non-dominant arm of right-handers. Our results indicate a similar pattern, but reduced lateralization for intersegmental coordination in left-handers. These findings suggest that left-handers develop more coordinated control of their non-dominant arms than right-handers, possibly due to environmental pressure for right-handed manipulations.     

Head movement control in visually guided tasks: postural goal and optimality

This work investigates the control of horizontal head movements in the context of unconstrained visually guided head and arm/finger aiming tasks. In a first experiment, the head was free to move while gaze was directed at randomly presented eccentric targets distributed horizontally (0 degrees-120 degrees) at eye level. In a second experiment, the horizontal head orientation was constrained to predetermined positions (0 degrees, 15 degrees, 30 degrees, 45 degrees or 60 degrees rightward) while the right index finger aimed at targets with the arm fully extended. Kinematics of head movements in gaze displacements exhibits an initial component weakly correlated with target position, followed by multiple corrections. Since the eyes are assumed to already be aimed at the target when the corrections occur, it is suggested that one goal of head movement control is to achieve a desired final orientation (posture). This hypothesis is supported by results from the second experiment that reveal an association between eye/head orientation angles and errors exhibited in the visuo-spatial representation of the environment. The minimization of error then underlies the control of head movement as a postural response optimized for a given target and task condition.     

Reaching during virtual rotation: context specific compensations for expected coriolis forces

Subjects who are in an enclosed chamber rotating at constant velocity feel physically stationary but make errors when pointing to targets. Reaching paths and endpoints are deviated in the direction of the transient inertial Coriolis forces generated by their arm movements. By contrast, reaching movements made during natural, voluntary torso rotation seem to be accurate, and subjects are unaware of the Coriolis forces generated by their movements. This pattern suggests that the motor plan for reaching movements uses a representation of body motion to prepare compensations for impending self-generated accelerative loads on the arm. If so, stationary subjects who are experiencing illusory self-rotation should make reaching errors when pointing to a target. These errors should be in the direction opposite the Coriolis accelerations their arm movements would generate if they were actually rotating. To determine whether such compensations exist, we had subjects in four experiments make visually open-loop reaches to targets while they were experiencing compelling illusory self-rotation and displacement induced by rotation of a complex, natural visual scene. The paths and endpoints of their initial reaching movements were significantly displaced leftward during counterclockwise illusory rotary displacement and rightward during clockwise illusory self-displacement. Subjects reached in a curvilinear path to the wrong place. These reaching errors were opposite in direction to the Coriolis forces that would have been generated by their arm movements during actual torso rotation. The magnitude of path curvature and endpoint errors increased as the speed of illusory self-rotation increased. In successive reaches, movement paths became straighter and endpoints more accurate despite the absence of visual error feedback or tactile feedback about target location. When subjects were again presented a stationary scene, their initial reaches were indistinguishable from pre-exposure baseline, indicating a total absence of aftereffects. These experiments demonstrate that the nervous system automatically compensates in a context-specific fashion for the Coriolis forces associated with reaching movements.     

Dissociable distal and proximal motor components: Evidence from perseverative errors in three apraxic patients

In the present study we analysed the perseverative behaviour of three apraxic patients (FG, CEO, and VCR) while they were pantomiming the use of common objects and during their real use. The three patients were found to perseverate from one trial to later ones aspects of a given action in the pantomiming and in real use tasks. In particular, our main result was a striking double dissociation between patients in perseverating hand and arm movements. Patients FG and CEO made more perseveration errors involving the hand than VCR did, whereas the perseverative errors made by VCR involving the arm were more numerous than those made by FG and CEO. The patients differed also in other aspects of the perseverations, e.g., their median lags. Results are used to exend previous theories developed in the linguistic domain to that of actions.     

Dissociable distal and proximal motor components: Evidence from perseverative errors in three apraxic patients

In the present study we analysed the perseverative behaviour of three apraxic patients (FG, CEO, and VCR) while they were pantomiming the use of common objects and during their real use. The three patients were found to perseverate from one trial to later ones aspects of a given action in the pantomiming and in real use tasks. In particular, our main result was a striking double dissociation between patients in perseverating hand and arm movements. Patients FG and CEO made more perseveration errors involving the hand than VCR did, whereas the perseverative errors made by VCR involving the arm were more numerous than those made by FG and CEO. The patients differed also in other aspects of the perseverations, e.g., their median lags. Results are used to exend previous theories developed in the linguistic domain to that of actions.     

Position sense at the human forearm in the horizontal plane during loading and vibration of elbow muscles

When blindfolded subjects match the position of their forearms in the vertical plane they rely on signals coming from the periphery as well as from the central motor command. The command signal provides a positional cue from the accompanying effort sensation required to hold the arm against gravity. Here we have asked, does a centrally generated effort signal contribute to position sense in the horizontal plane, where gravity cannot play a role? Blindfolded subjects were required to match forearm position for the unloaded arm and when flexors or extensors were bearing 10%, 25% or 40% of maximum loads. Before each match the reference arm was conditioned by contracting elbow muscles while the arm was held flexed or extended. For the unloaded arm conditioning led to a consistent pattern of errors which was attributed to signals from flexor and extensor muscle spindles. When elbow muscles were loaded the errors from conditioning converged, presumably because the spindles had become coactivated through the fusimotor system during the load-bearing contraction. However, this convergence was seen only when subjects supported a static load. When they moved the load differences in errors from conditioning persisted. Muscle vibration during load bearing or moving a load did not alter the distribution of errors. It is concluded that for position sense of an unloaded arm in the horizontal plane the brain relies on signals from muscle spindles. When the arm is loaded, an additional signal of central origin contributes, but only if the load is moved.     

The deafferented reticular thalamic nucleus generates spindle rhythmicity

The hypothesis that nucleus reticularis thalami (RE) is the generator of spindle rhythmicity during electroencephalogram (EEG) synchronization was tested in acutely prepared cats. Unit discharges and focal waves were extracellularly recorded in the rostral pole of RE nucleus, which was completely disconnected by transections from all other thalamic nuclei. In some experiments, additional transections through corona radiata created a triangular island in which the rostral RE pole survived with the caudate nucleus, putamen, basal forebrain nuclei, prepyriform area, and the adjacent cortex. Similar results were obtained in two types of experiments: brain stem-transected preparations that exhibited spontaneous spindle sequences, and animals under ketamine anesthesia in which transient spindling was repeatedly precipitated during recording by very low doses of a short-acting barbiturate. Both spindle-related rhythms (7- to 16-Hz waves grouped in sequences that recur with a rhythm of 0.1-0.3 Hz) are seen in focal recordings of the deafferented RE nucleus. The presence of spindling rhythmicity in the disconnected RE nucleus contrasts with total absence of spindles in cortical EEG leads and in thalamic recordings behind the transection. Oscillations within the same frequency range as that of spontaneous spindles can be evoked in the deafferented RE nucleus by subcortical white matter stimulation. In deafferented RE cells, the burst structure consists of an initially biphasic acceleration-deceleration pattern, eventually leading to a long-lasting tonic tail. Quantitative group data show that the burst parameters of disconnected RE cells are very similar to those of RE neurons with intact connections. In the deafferented RE nucleus, spike bursts of RE neurons recur periodically (0.1-0.3 Hz) in close time-relation with simultaneously recorded focal spindle sequences. The burst occurrence of deafferented RE cells is greatly reduced after systemic administration of bicuculline. The preservation of both spindle-related rhythms in the disconnected RE nucleus, together with our recent experiments showing abolition of spindle oscillations in thalamic nuclei after lesions of RE nucleus (24), demonstrate that RE nucleus is the generator of spindle rhythms.     

The role of proprioception and attention in a visuomotor adaptation task

The role of proprioception in the control and adaptation of visuomotor relationships is still unclear. We have studied a deafferented subject, IW, and control subjects in a task in which they used single joint elbow extension to move to a visual target, with visual feedback of the terminal position provided by a cursor displayed in the plane of their movements. We report the differences in movement accuracy between the deafferented subject and controls in the normal task and when challenged with a cognitive load, counting backwards. All subjects were less accurate when counting; this was a small effect for the controls (<10% change) but much greater for the deafferented subject (>60% change). We also examined changes in movement kinematics when the instructed amplitude was altered via a changed gain between final arm position and presentation of the feedback cursor. The deafferented subject maintained temporal movement parameters stable and altered amplitude by scaling force (i.e. changed peak velocity), whereas the controls scaled both movement velocity and duration. Finally, we compared the subjects' adaptation of movement amplitude after a period of exposure to the changed visuomotor gain. The deafferented subject was able to adapt, but his adaptation was severely impaired by the counting task. These results suggest that proprioception is not an absolute requirement for adaptation to occur. Instead, proprioception has a more subtle role to play in the adjustment to visuomotor perturbations. It has an important role in the control of reaching movements, while in the absence of proprioception, attention appears necessary to monitor movements.     

Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position

We recently provided evidence that the dominant and nondominant arms are specialized for controlling different aspects of reaching movements. In this study, we test whether these specializations lead to qualitatively different adaptive mechanisms, when exposed to novel inertial dynamics. Two groups of six right-handed adults performed a reaching task toward a single target with either the dominant or nondominant arm. After 39 trials of task familiarization without a load, subjects performed 180 trials with a 1.5 kg mass, positioned 25 cm lateral to the forearm. To assess the time course of adaptation, we quantified changes in movement direction and linearity, and to assess the quality of adaptation, we randomly interspersed aftereffect trials and generalization trials. The former were assessed by removing the mass and the latter by changing the location of the movement in the workspace. Whereas, final position accuracy improved to the same extent for both arms, initial movement direction improved only for the dominant arm. In contrast, nondominant arm adaptation occurred mainly by making more effective corrections for persistent errors in initial direction. Consistent with these findings, aftereffect trials, an indicator of feedforward control processes, showed progressive increases in error for only the dominant arm. In addition, substantial generalization only occurred for the dominant arm. These results support our hypothesis that interlimb differences in control mechanisms produce different patterns of adaptation to novel inertial dynamics.     

Disruptions in the reach-to-grasp actions of Parkinson's patients

Previous research has shown that Parkinson's-disease (PD) patients produce irregular movement paths during a rapid arm pointing task. The aim of this study was to investigate the movement paths of PD patients during a prehensile action to objects requiring different levels of precision. Thus, we sought to determine if movement-accuracy requirements affect the control of movement path. Thirteen PD patients and 13 age-matched controls served as participants. In addition to having prolonged movement times, PD patients showed differences in the kinematic patterns of the transport and grasp components. For the transport component, relative time to maximum deceleration and relative time to maximum elbow velocity occurred earlier for the PD patients than the controls. Analyses of wrist paths indicated that, when accuracy requirements were increased, patients produced paths that appeared more segmented than controls. For PD patients, reaches to a small object resulted in wrist paths that were significantly less smooth, as reflected by higher jerk values, and were less continuous, as indicated by larger standard deviations in curvature. A temporal analysis of movement-initiation patterns in the vertical and horizontal planes indicated that control participants had a minimal offset between initial movement in the vertical plane and initial movement in the horizontal plane regardless of accuracy constraints. However, PD patients had a significantly longer interval between initial movement in the vertical plane and subsequent movement in the horizontal plane when reaching to the small object. Higher accuracy constraints also resulted in PD patients achieving relative time to maximum elbow velocity significantly earlier than controls. For the grasp component, PD patients produced movement patterns in which the amplitude of and relative time to maximum aperture were less sensitive to object size. In addition, patients exhibited greater variability in the time to maximum aperture. Additional analyses of the grasp component indicated that control participants exhibited a stable position, relative to object location, in which aperture began to close. Conversely, PD patients showed little consistency in where aperture began to close with respect to object location. Irregularities in the transport component suggest that PD patients have a reduced capability to precisely coordinate joint segments, particularly under high accuracy requirements. Variability in where aperture began to close and disruptions in transport-grasp coordination suggests that the basal-ganglia dysfunction, as exhibited in PD, affects the specification of these movement parameters used to produce a consistent pattern of coordination between prehensile components.     

A systematic directional error in 2-D arm movements increases with increasing delay between visual target presentation and movement execution

Forty-seven normal subjects performed two-dimensional arm movements on a digitizer board using a mouse device. The movements were projected on a computer monitor. Subjects were instructed to move the mouse using the whole arm from a center position to a peripheral target so that the projected movement would pass over the target without stopping on the target. A large number of targets (360) were used to cover the entire directional continuum. The direction of the arm movement was the parameter of interest, which was measured at an initial position, at one third of the distance towards the target, and at the vicinity of the target. Four conditions of delay between target presentation and movement execution were used (0, 2, 4, 6 s). A systematic directional error was observed at the initial portion of the trajectory. This error resulted from a clustering of movement directions on an axis that was perpendicular to the axis of the resting forearm before movement onset. This pattern of errors can be explained by the initial inertial anisotropy of the arm. As the trajectory evolved, a different directional error emerged, resulting from a clustering of movement directions in two orthogonal axes. This pattern of directional error increased in amplitude as the delay increased, in contrast to the error at the initial portion of the trajectory which remained invariant with increasing delay. Finally, the information transmitted by the movement direction was shown to increase with the evolution of the trajectory. The increase in delay resulted in a decrease in directional-information transmission. It is proposed that the directional bias towards the end of the movement trajectory might reflect the action of "movement primitives", that is patterns of muscle activation resulting from spinal interneuronal activation. It is further proposed that the directional bias observed at the vicinity of the target might reflect a loss of cortical directional information with increasing delay between target presentation and movement onset.     

Instruction-related changes of neuronal activity in area 5 during a simple forearm movement in the monkey

Unit recordings were made in area 5 of monkeys during the performance of a sound-triggered movement of the forearm. Changes in neuronal activity prior to the movement were observed in 188 neurons recorded in both normal and deafferented animals. When the discharge of these cells was analyzed as peristimulus histograms, it was seen that 152 neurons presented a pattern of discharge which was characterized by a brief modification in activity with a relatively constant latency after the auditory cue. Similar changes were observed in normal and deafferented animals but the latency was not the same for the two groups. These neurons may reflect the presence of a sensorimotor interface for the integration of instructions for movement and the subsequent genesis of motor commands.     

Human forearm position sense after fatigue of elbow flexor muscles

After a period of eccentric exercise of elbow flexor muscles of one arm in young, adult human subjects, muscles became fatigued and damaged. Damage indicators were a fall in force, change in resting elbow angle and delayed onset of soreness. After the exercise, subjects were asked to match the forearm angle of one arm, whose position was set by the experimenter, with their other arm. Subjects matched the position of the unsupported reference arm, when this was unexercised, with a significantly more flexed position in their exercised indicator arm. Errors were in the opposite direction when the reference arm was exercised. The size of the errors correlated with the drop in force. Less consistent errors were observed when the reference arm was supported. A similar pattern of errors was seen after concentric exercise, which does not produce muscle damage. The data suggested that subjects were using as a position cue the perceived effort required to maintain a given forearm angle against the force of gravity. The fall in force from fatigue after exercise meant more effort was required to maintain a given position. That led to matching errors between the exercised and unexercised arms. It was concluded that while a role for muscle spindles in kinaesthesia cannot be excluded, detailed information about static limb position can be derived from the effort required to support the limb against the force of gravity.     

Does the oculo-manual co-ordination control system use an internal model of the arm dynamics?

The hypothesis that during self-moved target tracking, the eye-arm co-ordination control system uses an internal model of the arm dynamics was tested. The contribution of arm proprioception to this model was also assessed. Subjects (nine healthy adults and one deafferented subject) were requested to make forearm movements and visually track an arm-driven target. Unexpected changes in mechanical properties of the manipulandum were used to modify the dynamical conditions of arm movement. The smooth pursuit gain (SPG) was computed before and during the perturbation. Results showed a decrease of SPG during perturbation in control subjects only. We propose that an internal model of the arm dynamics may be used to co-ordinate eye and arm movements, and arm proprioception may contribute to this internal model.     

Evidence for stronger visuo-motor than visuo-proprioceptive conflict during mirror drawing performed by a deafferented subject and control subjects

It has been proposed that mirror drawing is difficult because of the conflict between visual and proprioceptive signals from the arm. However, even without proprioception, there should be difficulties in planning movements to visual targets observed in a mirror, as the mirror-reversed spatial information must be translated into appropriate hand actions. Mirror drawing tasks suggest these planning conflicts are likely to be most obvious at corners, when encountering sharp changes in direction. We have therefore tested the speed of mirror drawing in a chronically deafferented man and in a control group of normal subjects, and hypothesized that increases in template complexity (number of corners) would result in reduced drawing speeds in all subjects. Indeed, all subjects, including the deafferented man, showed movement durations that increased linearly as the complexity of the drawings increased. However, the deafferented man was significantly faster than the control subjects at tracing curved templates. We suggest that the major difficulty in mirror tracking is in the visuo-motor planning of actions based on mirror-reversed visual information, and is not a conflict between visual and proprioceptive signals about arm motion.