A neural mechanism for coordinate transformation predicts pre-saccadic remapping

Whenever we shift our gaze, any location information encoded in the retinocentric reference frame that is predominant in the visual system is obliterated. How is spatial memory retained across gaze changes? Two different explanations have been proposed: Retinocentric information may be transformed into a gaze-invariant representation through a mechanism consistent with gain fields observed in parietal cortex, or retinocentric information may be updated in anticipation of the shift expected with every gaze change, a proposal consistent with neural observations in LIP. The explanations were considered incompatible with each other, because retinocentric update is observed before the gaze shift has terminated. Here, we show that a neural dynamic mechanism for coordinate transformation can also account for retinocentric updating. Our model postulates an extended mechanism of reference frame transformation that is based on bidirectional mapping between a retinocentric and a body-centered representation and that enables transforming multiple object locations in parallel. The dynamic coupling between the two reference frames generates a shift of the retinocentric representation for every gaze change. We account for the predictive nature of the observed remapping activity by using the same kind of neural mechanism to generate an internal representation of gaze direction that is predictively updated based on corollary discharge signals. We provide evidence for the model by accounting for a series of behavioral and neural experimental observations.     

Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning

When reaching to grasp an object, we often move our arm and orient our gaze together. How are these movements coordinated? To investigate this question, we studied neuronal activity in the dorsal premotor area (PMd) and the medial intraparietal area (area MIP) of two monkeys while systematically varying the starting position of the hand and eye during reaching. PMd neurons encoded the relative position of the target, hand, and eye. MIP neurons encoded target location with respect to the eye only. These results indicate that whereas MIP encodes target locations in an eye-centered reference frame, PMd uses a relative position code that specifies the differences in locations between all three variables. Such a relative position code may play an important role in coordinating hand and eye movements by computing their relative position.     

Where the eye looks, the hand follows; limb-dependent magnetic misreaching in optic ataxia

The posterior parietal cortex (PPC) is thought to play an important role in the sensorimotor transformations associated with reaching movements. In humans, damage to the PPC, particularly bilateral lesions, leads to impairments of visually guided reaching movements (optic ataxia). Recent accounts of optic ataxia based upon electrophysiological recordings in monkeys have proposed that this disorder arises because of a breakdown in the tuning fields of parietal neurons responsible for integrating spatially congruent retinal, eye, and hand position signals to produce coordinated eye and hand movements . We present neurological evidence that forces a reconceptualization of this view. We report a detailed case study of a patient with a limb-dependent form of optic ataxia who can accurately reach with either hand to objects that he can foveate (thereby demonstrating coordinated eye-hand movements) but who cannot effectively decouple reach direction from gaze direction for movements executed using his right arm. The demonstration that our patient's misreaching is confined to movements executed using his right limb, and only for movements that are directed to nonfoveal targets, rules out explanations based upon simple perceptual or motor deficits but indicates an impairment in the ability to dissociate the eye and limb visuomotor systems when appropriate.     

Flexible representations of dynamics are used in object manipulation

To manipulate an object skillfully, the brain must learn its dynamics, specifying the mapping between applied force and motion. A fundamental issue in sensorimotor control is whether such dynamics are represented in an extrinsic frame of reference tied to the object or an intrinsic frame of reference linked to the arm. Although previous studies have suggested that objects are represented in arm-centered coordinates [1-6], all of these studies have used objects with unusual and complex dynamics. Thus, it is not known how objects with natural dynamics are represented. Here we show that objects with simple (or familiar) dynamics and those with complex (or unfamiliar) dynamics are represented in object- and arm-centered coordinates, respectively. We also show that objects with simple dynamics are represented with an intermediate coordinate frame when vision of the object is removed. These results indicate that object dynamics can be flexibly represented in different coordinate frames by the brain. We suggest that with experience, the representation of the dynamics of a manipulated object may shift from a coordinate frame tied to the arm toward one that is linked to the object. The additional complexity required to represent dynamics in object-centered coordinates would be economical for familiar objects because such a representation allows object use regardless of the orientation of the object in hand.     

Uniqueness of primate forelimb posture during quadrupedal locomotion

Among the characteristics that are thought to set primate quadrupedal locomotion apart from that of nonprimate mammals are a more protracted limb posture and larger limb angular excursion. However, kinematic aspects of primate or nonprimate quadrupedal locomotion have been documented in only a handful of species, and more widely for the hind than the forelimb. This study presents data on arm (humerus) and forelimb posture during walking for 102 species of mammals, including 53 nonhuman primates and 49 nonprimate mammals. The results demonstrate that primates uniformly display a more protracted arm and forelimb at hand touchdown of a step than nearly all other mammals. Although primates tend to end a step with a less retracted humerus, their total humeral or forelimb angular excursion exceeds that of other mammals. It is suggested that these features are components of functional adaptations to locomotion in an arboreal habitat, using clawless, grasping extremities.     

Arm-plane representation of shoulder compensation during pointing movements in patients with stroke

Improvements in functional motor activities are often accompanied by motor compensations to overcome persistent motor impairment in the upper limb. Kinematic analysis is used to objectively quantify movement patterns including common motor compensations such as excessive trunk displacement during reaching. However, a common motor compensation to assist reaching, shoulder abduction, is not adequately characterized by current motion analysis approaches. We apply the arm-plane representation that accounts for the co-variation between movements of the whole arm, and investigate its ability to identify and quantify compensatory arm movements in stroke subjects when making forward arm reaches. This method has not been previously applied to the analysis of motion deficits. Sixteen adults with right post-stroke hemiparesis and eight healthy age-matched controls reached in three target directions (14 trials/target; sampling rate: 100 Hz). Arm-plane movement was validated against endpoint, joint, and trunk kinematics and compared between groups. In stroke subjects, arm-plane measures were correlated with arm impairment (Fugl-Meyer Assessment) and ability (Box and Blocks) scores and were more sensitive than clinical measures to detect mild motor impairment. Arm-plane motion analysis provides new information about motor compensations involving the co-variation of shoulder and elbow movements that may help to understand the underlying motor deficits in patients with stroke.     

Use of Self-Selected Postures to Regulate Multi-Joint Stiffness During Unconstrained Tasks

Background

The human motor system is highly redundant, having more kinematic degrees of freedom than necessary to complete a given task. Understanding how kinematic redundancies are utilized in different tasks remains a fundamental question in motor control. One possibility is that they can be used to tune the mechanical properties of a limb to the specific requirements of a task. For example, many tasks such as tool usage compromise arm stability along specific directions. These tasks only can be completed if the nervous system adapts the mechanical properties of the arm such that the arm, coupled to the tool, remains stable. The purpose of this study was to determine if posture selection is a critical component of endpoint stiffness regulation during unconstrained tasks.

Methodology/Principal Findings

Three-dimensional (3D) estimates of endpoint stiffness were used to quantify limb mechanics. Most previous studies examining endpoint stiffness adaptation were completed in 2D using constrained postures to maintain a non-redundant mapping between joint angles and hand location. Our hypothesis was that during unconstrained conditions, subjects would select arm postures that matched endpoint stiffness to the functional requirements of the task. The hypothesis was tested during endpoint tracking tasks in which subjects interacted with unstable haptic environments, simulated using a 3D robotic manipulator. We found that arm posture had a significant effect on endpoint tracking accuracy and that subjects selected postures that improved tracking performance. For environments in which arm posture had a large effect on tracking accuracy, the self-selected postures oriented the direction of maximal endpoint stiffness towards the direction of the unstable haptic environment.

Conclusions/Significance

These results demonstrate how changes in arm posture can have a dramatic effect on task performance and suggest that postural selection is a fundamental mechanism by which kinematic redundancies can be exploited to regulate arm stiffness in unconstrained tasks.     

Coding of the reach vector in parietal area 5d

Competing models of sensorimotor computation predict different topological constraints in the brain. Some models propose population coding of particular reference frames in anatomically distinct nodes, whereas others require no such dedicated subpopulations and instead predict that regions will simultaneously code in multiple, intermediate, reference frames. Current empirical evidence is conflicting, partly due to difficulties involved in identifying underlying reference frames. Here, we independently varied the locations of hand, gaze, and target over many positions while recording from the dorsal aspect of parietal area 5. We find that the target is?represented in a predominantly hand-centered reference frame here, contrasting with the relative code seen in dorsal premotor cortex and the mostly gaze-centered reference frame in the parietal reach region. This supports the hypothesis that different nodes of the sensorimotor circuit contain distinct and systematic representations, and this constrains the types of computational model that are neurobiologically relevant.     

The Role of the Caudal Superior Parietal Lobule in Updating Hand Location in Peripheral Vision: Further Evidence from Optic Ataxia

Patients with optic ataxia (OA), who are missing the caudal portion of their superior parietal lobule (SPL), have difficulty performing visually-guided reaches towards extra-foveal targets. Such gaze and hand decoupling also occurs in commonly performed non-standard visuomotor transformations such as the use of a computer mouse. In this study, we test two unilateral OA patients in conditions of 1) a change in the physical location of the visual stimulus relative to the plane of the limb movement, 2) a cue that signals a required limb movement 180° opposite to the cued visual target location, or 3) both of these situations combined. In these non-standard visuomotor transformations, the OA deficit is not observed as the well-documented field-dependent misreach. Instead, OA patients make additional eye movements to update hand and goal location during motor execution in order to complete these slow movements. Overall, the OA patients struggled when having to guide centrifugal movements in peripheral vision, even when they were instructed from visual stimuli that could be foveated. We propose that an intact caudal SPL is crucial for any visuomotor control that involves updating ongoing hand location in space without foveating it, i.e. from peripheral vision, proprioceptive or predictive information.     

Organization of space perception: neural representation of three-dimensional space in the posterior parietal cortex.

The representation of perceptual space in the posterior parietal cortex can be divided into at least two categories: far space, beyond arm's reach, and peripersonal space, within arm's reach. These are encoded by different groups of neurons that are closely related to the control of gaze and the guidance of arm and hand movement, respectively.     

Learning robotic eye–arm–hand coordination from human demonstration: a coupled dynamical systems approach

We investigate the role of obstacle avoidance in visually guided reaching and grasping movements. We report on a human study in which subjects performed prehensile motion with obstacle avoidance where the position of the obstacle was systematically varied across trials. These experiments suggest that reaching with obstacle avoidance is organized in a sequential manner, where the obstacle acts as an intermediary target. Furthermore, we demonstrate that the notion of workspace travelled by the hand is embedded explicitly in a forward planning scheme, which is actively involved in detecting obstacles on the way when performing reaching. We find that the gaze proactively coordinates the pattern of eye–arm motion during obstacle avoidance. This study provides also a quantitative assessment of the coupling between the eye–arm–hand motion. We show that the coupling follows regular phase dependencies and is unaltered during obstacle avoidance. These observations provide a basis for the design of a computational model. Our controller extends the coupled dynamical systems framework and provides fast and synchronous control of the eyes, the arm and the hand within a single and compact framework, mimicking similar control system found in humans. We validate our model for visuomotor control of a humanoid robot.     

Virtual musculo-skeletal model for the biomechanical analysis of the upper limb

In this paper, a musculo-skeletal model of the upper limb is presented. The limb is modelled as a three-dimensional 7 degrees-of-freedom system, linked to the shoulder, which has been considered as frame. The upper limb model is made up of four links corresponding to the most important body segments: the humerus, the ulna, the radius and the hand, considered as a single rigid body. Particular attention has been paid to the modelling of joints in order to mimic all the possible arm and forearm movements (including prono-supination). The model also includes 24 muscles. The mathematical model used to describe the muscles is that proposed by Zajac in 1989, modified by the authors. The kinematic analysis has been performed including an ergonomics index to take into account the posture and joint physical limits. Moreover an optimization criterion based on minimum activation pattern has been included in order to find muscular activation coefficients. The results of the proposed methodology concerning muscular activations have been compared to those coming from processed EMG signals, which have been acquired during experimental tests.     

Learning visuomotor transformations for gaze-control and grasping

For reaching to and grasping of an object, visual information about the object must be transformed into motor or postural commands for the arm and hand. In this paper, we present a robot model for visually guided reaching and grasping. The model mimics two alternative processing pathways for grasping, which are also likely to coexist in the human brain. The first pathway directly uses the retinal activation to encode the target position. In the second pathway, a saccade controller makes the eyes (cameras) focus on the target, and the gaze direction is used instead as positional input. For both pathways, an arm controller transforms information on the target’s position and orientation into an arm posture suitable for grasping. For the training of the saccade controller, we suggest a novel staged learning method which does not require a teacher that provides the necessary motor commands. The arm controller uses unsupervised learning: it is based on a density model of the sensor and the motor data. Using this density, a mapping is achieved by completing a partially given sensorimotor pattern. The controller can cope with the ambiguity in having a set of redundant arm postures for a given target. The combined model of saccade and arm controller was able to fixate and grasp an elongated object with arbitrary orientation and at arbitrary position on a table in 94% of trials.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.     

Planning movements in a simple redundant task

There are infinitely many different combinations of arm postures which will place the hand at the same point in space. Given this abundance, how is one configuration chosen over another? Two main hypotheses have been proposed to solve this problem. Postural models suggest that the posture adopted is purely determined by the desired hand position (known as Donders' law). Transport models suggest that the adopted posture depends on where the hand has moved from. A specific transport model, the minimum work model, has been proposed in which the adopted posture is the one that minimizes the amount of work required to move the hand to the new location. The postural model predicts that the posture will be independent of where the hand has moved from, whereas the transport models predict that the posture will depend on the previous posture. We have devised a simple redundant task-touching a target bar using a hand-held virtual stick-to examine these models. The results show that neither model alone can account for the data. We propose a control planning strategy in which there is a combined cost function that has both a postural term as well as a transport term.     

Biomechanical outcomes and neural correlates of cutaneous reflexes evoked during rhythmic arm cycling

During walking cutaneous stimulation of the foot yields neural and mechanical reflexes that serve a functional purpose to correct or assist the ongoing movement. Concurrently, while cutaneous stimulation of the hand during rhythmic arm movement parallel the neural responses observed in the legs, studies of rhythmic arm movement have only limited mechanical measurements. Therefore it is difficult to determine whether reflex responses in the arms during rhythmic arm movement serve a functional purpose similar to those seen in the lower limbs. The purpose of this study was to explore the mechanical outcomes of stimulating a cutaneous nerve innervating the hand during arm cycling. We hypothesized that there would be measurable mechanical effects to cutaneous stimulation during arm cycling that function to correct or assist the task of arm cycling. Specifically, kinetic responses measured at the handle would be considered assistive if they were tangential to the arm cycling path in the direction of forward progression. Also, limb kinematic responses would be considered corrective if they allowed limb movement that would result in removal of the limb from stimulus while not altering the kinetic profile at the handle necessary for arm cycling progression. Participants performed seated arm cycling while EMG was recorded from the arm and trunk muscles, kinematic data was recorded from the right arm, and kinetic data was recorded from the handle. Cutaneous reflexes were evoked by stimulating the superficial radial nerve. The results show that there are observable mechanical responses to cutaneous stimulation of the hand during arm cycling. Subjects responded to cutaneous stimulation of the hand during arm cycling with significant changes in backward and lateral forces at the handle as well as wrist abduction/adduction and wrist flexion/extension kinematics. These responses, related to the task and phase of movement, are consistent with the anatomical location of the stimulus and are correlated to the neural responses. Therefore, these responses are comparable to functionally relevant responses in the legs during rhythmic movement. However, while there is a single observation of a kinematic corrective strategy, the kinetics measured at the handle are not tangential to the arm cycling path and therefore not considered an assistive response. Therefore, unlike the observations in the lower limbs, the mechanical responses during arm cycling are not clearly related to the functional context of the ongoing task.     

Decoupled Visually-Guided Reaching in Optic Ataxia: Differences in Motor Control between Canonical and Non-Canonical Orientations in Space

Guiding a limb often involves situations in which the spatial location of the target for gaze and limb movement are not congruent (i.e. have been decoupled). Such decoupled situations involve both the implementation of a cognitive rule (i.e. strategic control) and the online monitoring of the limb position relative to gaze and target (i.e. sensorimotor recalibration). To further understand the neural mechanisms underlying these different types of visuomotor control, we tested patient IG who has bilateral caudal superior parietal lobule (SPL) damage resulting in optic ataxia (OA), and compared her performance with six age-matched controls on a series of center-out reaching tasks. The tasks comprised 1) directing a cursor that had been rotated (180° or 90°) within the same spatial plane as the visual display, or 2) moving the hand along a different spatial plane than the visual display (horizontal or para-sagittal). Importantly, all conditions were performed towards visual targets located along either the horizontal axis (left and right; which can be guided from strategic control) or the diagonal axes (top-left and top-right; which require on-line trajectory elaboration and updating by sensorimotor recalibration). The bilateral OA patient performed much better in decoupled visuomotor control towards the horizontal targets, a canonical situation in which well-categorized allocentric cues could be utilized (i.e. guiding cursor direction perpendicular to computer monitor border). Relative to neurologically intact adults, IG''s performance suffered towards diagonal targets, a non-canonical situation in which only less-categorized allocentric cues were available (i.e. guiding cursor direction at an off-axis angle to computer monitor border), and she was therefore required to rely on sensorimotor recalibration of her decoupled limb. We propose that an intact caudal SPL is crucial for any decoupled visuomotor control, particularly when relying on the realignment between vision and proprioception without reliable allocentric cues towards non-canonical orientations in space.     

Gaze control: role of the parietal cortex

Eye movements constitute one of the most basic means of interacting with our environment, allowing to orient to, localize and scrutinize the variety of potentially interesting objects that surround us. In this review we discuss the role of the parietal cortex in the control of saccadic and smooth pursuit eye movements, whose purpose is to rapidly displace the line of gaze and to maintain a moving object on the central retina, respectively. From single cell recording studies in monkey we know that distinct sub-regions of the parietal lobe are implicated in these two kinds of movement. The middle temporal (MT) and medial superior temporal (MST) areas show neuronal activities related to moving visual stimuli and to ocular pursuit. The lateral intraparietal (LIP) area exhibits visual and saccadic neuronal responses. Electrophysiology, which in essence is a correlation method, cannot entirely solve the question of the functional implication of these areas: are they primarily involved in sensory processing, in motor processing, or in some intermediate function? Lesion approaches (reversible or permanent) in the monkey can provide important information in this respect. Lesions of MT or MST produce deficits in the perception of visual motion, which would argue for their possible role in sensory guidance of ocular pursuit rather than in directing motor commands to the eye muscle. Lesions of LIP do not produce specific visual impairments and cause only subtle saccadic deficits. However, recent results have shown the presence of severe deficits in spatial attention tasks. LIP could thus be implicated in the selection of relevant objects in the visual scene and provide a signal for directing the eyes toward these objects. Functional imaging studies in humans confirm the role of the parietal cortex in pursuit, saccadic, and attentional networks, and show a high degree of overlap with monkey data. Parietal lobe lesions in humans also result in behavioral deficits very similar to those that are observed in the monkey. Altogether, these different sources of data consistently point to the involvement of the parietal cortex in the representation of space, at an intermediate stage between vision and action.     

Catching a ball at the right time and place: individual factors matter

Intercepting a moving object requires accurate spatio-temporal control. Several studies have investigated how the CNS copes with such a challenging task, focusing on the nature of the information used to extract target motion parameters and on the identification of general control strategies. In the present study we provide evidence that the right time and place of the collision is not univocally specified by the CNS for a given target motion; instead, different but equally successful solutions can be adopted by different subjects when task constraints are loose. We characterized arm kinematics of fourteen subjects and performed a detailed analysis on a subset of six subjects who showed comparable success rates when asked to catch a flying ball in three dimensional space. Balls were projected by an actuated launching apparatus in order to obtain different arrival flight time and height conditions. Inter-individual variability was observed in several kinematic parameters, such as wrist trajectory, wrist velocity profile, timing and spatial distribution of the impact point, upper limb posture, trunk motion, and submovement decomposition. Individual idiosyncratic behaviors were consistent across different ball flight time conditions and across two experimental sessions carried out at one year distance. These results highlight the importance of a systematic characterization of individual factors in the study of interceptive tasks.     

Postural response characterization of standing humans to multi-directional,predictable and unpredictable perturbations to the arm

When the arm of a standing human is perturbed in an unpredictable direction, postural muscles are activated at latencies as short as 50–110 ms. While the motion of the body clearly progresses in hand-to-leg sequence, there is no systematic muscle activation sequence from the arm to the leg muscles, suggesting that the activation of the muscles is not likely the result of local stretch reflexes. In fact, the lower limb muscles are activated before the upright posture is significantly disturbed. The short-latency activation amplitude and the activation probability are clearly tuned to the direction of the arm perturbation for both rostral and caudal muscles. The effect of central set on the short-latency response has been investigated by manipulating the predictability of the perturbations. Possible underlying neural mechanisms have been discussed.