Visuomotor Mechanisms Research Articles

Are reaching and grasping effector-independent? Similarities and differences in reaching and grasping kinematics between the hand and foot

While reaching and grasping are highly prevalent manual actions, neuroimaging studies provide evidence that their neural representations may be shared between different body parts, i.e., effectors. If these actions are guided by effector-independent mechanisms, similar kinematics should be observed when the action is performed by the hand or by a cortically remote and less experienced effector, such as the foot. We tested this hypothesis with two characteristic components of action: the initial ballistic stage of reaching, and the preshaping of the digits during grasping based on object size. We examined if these kinematic features reflect effector-independent mechanisms by asking participants to reach toward and to grasp objects of different widths with their hand and foot. First, during both reaching and grasping, the velocity profile up to peak velocity matched between the hand and the foot, indicating a shared ballistic acceleration phase. Second, maximum grip aperture and time of maximum grip aperture of grasping increased with object size for both effectors, indicating encoding of object size during transport. Differences between the hand and foot were found in the deceleration phase and time of maximum grip aperture, likely due to biomechanical differences and the participants’ inexperience with foot actions. These findings provide evidence for effector-independent visuomotor mechanisms of reaching and grasping that generalize across body parts.

Stereopsis contributes to the predictive control of grip forces during prehension.

Binocular viewing is associated with a superior prehensile performance, which is particularly evident in the latter part of the reach as the hand approaches and makes contact with the target object. However, the visuomotor mechanisms through which binocular vision serves prehension are not fully understood. This study assessed the role of stereopsis in the predictive control of grasping by measuring grip force. Twenty participants performed a precision reach-to-grasp task in four viewing conditions: binocular, monocular, and with reduced stereoacuity (200 arc sec, > 400 arc sec). Monocular, compared to binocular viewing, was associated with a fourfold increase in grasp errors, a 56% increase in grasp duration, 22% decrease in grip force at 50ms following grasp initiation, and the time of peak force occurred 40% later after grasp initiation (all p < 0.05). Grasp performance was also disrupted when viewing with reduced stereoacuity. Notably, grip force at the time of object lift-off was comparable between all viewing conditions. These results demonstrate that binocular stereopsis contributes to the efficient programming of grip forces. Specifically, stereopsis may provide important sensory information that enables the central nervous system to engage in predictive control of grasping.

Distinct temporal developments of visual motion and position representations for multi-stream visuomotor coordination

A fundamental but controversial question in information coding of moving visual target is which of ‘motion’ or ‘position’ signal is employed in the brain for producing quick motor reactions. Prevailing theory assumed that visually guided reaching is driven always via target position representation influenced by various motion signals (e.g., target texture and surroundings). To rigorously examine this theory, we manipulated the nature of the influence of internal texture motion on the position representation of the target in reaching correction tasks. By focusing on the difference in illusory position shift of targets with the soft- and hard-edges, we succeeded in extracting the temporal development of an indirect effect only ascribed to changes in position representation. Our data revealed that the onset of indirect effect is significantly slower than the adjustment onset itself. This evidence indicates multi-stream processing in visuomotor control: fast and direct contribution of visual motion for quick action initiation, and relatively slow contribution of position representation updated by relevant motion signals for continuous action regulation. The distinctive visuomotor mechanism would be crucial in successfully interacting with time-varying environments in the real world.

Rapid adjustment of pecking trajectory to prism-induced visual shifts in crows as compared with pigeons.

Pecking in birds is analogous to reaching and grasping movements in primates. Earlier studies on visuomotor control in birds, which were conducted mostly in pigeons, suggested that avian pecking is controlled feedforwardly, and is out of the control of visual guidance during movement. However, recent studies using crows suggested a role of vision in pecking control during movement. To unveil what visuomotor mechanisms underlie the flexibility of pecking in crows, we examined whether pigeons and crows adjust their pecking to the visual distortion induced by prisms. Because prisms induce visual shifts of object positions, birds were required to adjust their movements. Pecking kinematics were examined before and after attaching prisms in front of the birds' eyes. Analysis of lateral deviation caused by the prisms showed that crows rapidly adjusted their pecking trajectories, but pigeons did so slowly. Angular displacement also increased in pigeons after attachment of the prism, but decreased in crows. These responses to prisms were consistent among individuals in pigeons but varied in crows, though the adjustment of pecking commonly succeeded in crows. These results suggest that pecking in pigeons predominantly involves feedforward control and that the movement is determined depending on the visual information available before the initiation of pecking. In contrast, the results from crows suggest that their pecking trajectories are corrected during the movement, supporting on-line visual control. Our findings provide the first evidence to suggest the on-line visual control of pecking in birds.

Distinct and flexible rates of online control.

Elliott et al. (Hum Mov Sci 10:393-418, 1991) proposed a pseudocontinuous model of online control whereby overlapping corrections lead to the appearance of smooth kinematic profiles in the presence of online feedback. More recently, it was also proposed that online control is not a singular process [see Elliott et al. (Psychol Bull 136(6):1023-1044, 2010)]. However, support for contemporary models of online control were based on methodologies that were not designed to be sensitive to different online control sub-processes. The current study sought to evaluate the possibility of multiple distinct (i.e., visual and non-visual) mechanisms contributing to the control of reaching movements completed in either a full-vision, a no-vision, or a no-vision memory-guided condition. Frequency domain analysis was applied to the acceleration traces of reaching movements. In an attempt to elicit a modulation in the online control mechanisms, these movements were completed at two levels of spatio-temporal constraint, namely with 10 and 30cm target distances. One finding was that performance in the full-vision relative to both no-vision conditions could be distinguished via two distinct frequency peaks. Increases in the peak magnitude at the lower frequencies were associated with visuomotor mechanisms and increases in the peak magnitude at the higher frequencies were associated with non-visual mechanisms. In addition, performance to the 30-cm target led to a lower peak at a lower frequency relative to the 10 cm target, indicating that the iterative rates of visuomotor control mechanisms are flexible and sensitive to the spatio-temporal constraints of the associated movement.

A State Space Model for Spatial Updating of Remembered Visual Targets during Eye Movements.

In the oculomotor system, spatial updating is the ability to aim a saccade toward a remembered visual target position despite intervening eye movements. Although this has been the subject of extensive experimental investigation, there is still no unifying theoretical framework to explain the neural mechanism for this phenomenon, and how it influences visual signals in the brain. Here, we propose a unified state-space model (SSM) to account for the dynamics of spatial updating during two types of eye movement; saccades and smooth pursuit. Our proposed model is a non-linear SSM and implemented through a recurrent radial-basis-function neural network in a dual Extended Kalman filter (EKF) structure. The model parameters and internal states (remembered target position) are estimated sequentially using the EKF method. The proposed model replicates two fundamental experimental observations: continuous gaze-centered updating of visual memory-related activity during smooth pursuit, and predictive remapping of visual memory activity before and during saccades. Moreover, our model makes the new prediction that, when uncertainty of input signals is incorporated in the model, neural population activity and receptive fields expand just before and during saccades. These results suggest that visual remapping and motor updating are part of a common visuomotor mechanism, and that subjective perceptual constancy arises in part from training the visual system on motor tasks.

Feedforward and feedback motor control abnormalities implicate cerebellar dysfunctions in autism spectrum disorder.

Sensorimotor abnormalities are common in autism spectrum disorder (ASD) and among the earliest manifestations of the disorder. They have been studied far less than the social-communication and cognitive deficits that define ASD, but a mechanistic understanding of sensorimotor abnormalities in ASD may provide key insights into the neural underpinnings of the disorder. In this human study, we examined rapid, precision grip force contractions to determine whether feedforward mechanisms supporting initial motor output before sensory feedback can be processed are disrupted in ASD. Sustained force contractions also were examined to determine whether reactive adjustments to ongoing motor behavior based on visual feedback are altered. Sustained force was studied across multiple force levels and visual gains to assess motor and visuomotor mechanisms, respectively. Primary force contractions of individuals with ASD showed greater peak rate of force increases and large transient overshoots. Individuals with ASD also showed increased sustained force variability that scaled with force level and was more severe when visual gain was highly amplified or highly degraded. When sustaining a constant force level, their reactive adjustments were more periodic than controls, and they showed increased reliance on slower feedback mechanisms. Feedforward and feedback mechanism alterations each were associated with more severe social-communication impairments in ASD. These findings implicate anterior cerebellar circuits involved in feedforward motor control and posterior cerebellar circuits involved in transforming visual feedback into precise motor adjustments in ASD.

Involvement of vision in tool use in crow.

Birds are capable of dexterous sensory-motor activities such as tool use. Reaching is a crucial component of tool use and is a vision-guided behavior in primates, in which arm movement is monitored online in a stable visual frame. However, vision-guided reaching in primates is enabled by anatomical separation of the head and arm; neck reaching in birds accompanies head movement, which produces unstable vision because the eye necessarily moves with the bill. This anatomical difference raises the question whether tool use in birds involves visuomotor mechanisms that are distinct from those in primates. As the role of vision in avian tool use has been poorly understood, we investigated the role of vision in tool use in the large-billed crow (Corvus macrorhynchos), a nontool user in the wild. Crows were trained to manipulate an L-shaped hook to retrieve food that was otherwise out of reach. After training, an opaque panel was placed on the front window of the platform to block their vision, and the effects on tool use were tested with respect to performance and movement trajectory. Vision blocking caused similar deviation of tool movement trajectories for both near and far targets, as well as far target-specific deviation. This suggests the involvement of vision in tool use by crows, specifically in the premanipulation process for conversion of vision-body coordinates for motor planning and in the process of tool manipulation. This is the first behavioral evidence for the involvement of vision in avian tool use.

Optic Ataxia: From Balint’s Syndrome to the Parietal Reach Region

Optic ataxia is a high-order deficit in reaching to visual goals that occurs with posterior parietal cortex (PPC) lesions. It is a component of Balint's syndrome that also includes attentional and gaze disorders. Aspects of optic ataxia are misreaching in the contralesional visual field, difficulty preshaping the hand for grasping, and an inability to correct reaches online. Recent research in nonhuman primates (NHPs) suggests that many aspects of Balint's syndrome and optic ataxia are a result of damage to specific functional modules for reaching, saccades, grasp, attention, and state estimation. The deficits from large lesions in humans are probably composite effects from damage to combinations of these functional modules. Interactions between these modules, either within posterior parietal cortex or downstream within frontal cortex, may account for more complex behaviors such as hand-eye coordination and reach-to-grasp.

Training the Motor Cortex by Observing the Actions of Others During Immobilization

Limb immobilization and nonuse are well-known causes of corticomotor depression. While physical training can drive the recovery from nonuse-dependent corticomotor effects, it remains unclear if it is possible to gain access to motor cortex in alternative ways, such as through motor imagery (MI) or action observation (AO). Transcranial magnetic stimulation was used to study the excitability of the hand left motor cortex in normal subjects immediately before and after 10 h of right arm immobilization. During immobilization, subjects were requested either to imagine to act with their constrained limb or to observe hand actions performed by other individuals. A third group of control subjects watched a nature documentary presented on a computer screen. Hand corticomotor maps and recruitment curves reliably showed that AO, but not MI, prevented the corticomotor depression induced by immobilization. Our results demonstrate the existence of a visuomotor mechanism in humans that links AO and execution which is able to effect cortical plasticity in a beneficial way. This facilitation was not related to the action simulation, because it was not induced by explicit MI.

The effects of smooth pursuit adaptation on the gain of visuomotor transmission in monkeys

Smooth pursuit eye movements are supported by visual-motor systems, where visual motion information is transformed into eye movement commands. Adaptation of the visuomotor systems for smooth pursuit is an important factor to maintain pursuit accuracy and high acuity vision. Short-term adaptation of initial pursuit gain can be produced experimentally using by repeated trials of a step-ramp tracking with two different velocities (double-step paradigm) that step-up (10–30°/s) or step-down (20–5°/s). It is also known that visuomotor gain during smooth pursuit is regulated by a dynamic gain control mechanism by showing that eye velocity evoked by a target perturbation during pursuit increases bidirectionally when ongoing pursuit velocity is higher. However, it remains uncertain how smooth pursuit adaptation alters the gain of visuomotor transmission. Therefore, a single cycle of sinusoidal motion (2.5 Hz, ± 10°/s) was introduced during step-ramp tracking pre- and post-adaptation to determine whether smooth pursuit adaptation affects the perturbation response. The results showed that pursuit adaptation had a significant effect on the perturbation response that was specific to the adapted direction. These results indicate that there might be different visuomotor mechanisms between adaptation and dynamic gain control. Furthermore, smooth pursuit adaptation altered not only the gain of the perturbation response, but also the gain slope (regression curve) at different target velocities (5, 10 and 15°/s). Therefore, pursuit adaptation could affect the dynamic regulation of the visuomotor gain at different pursuit velocities.

Inactivation of the Parietal Reach Region Causes Optic Ataxia, Impairing Reaches but Not Saccades

Lesions in human posterior parietal cortex can cause optic ataxia (OA), in which reaches but not saccades to visual objects are impaired, suggesting separate visuomotor pathways for the two effectors. In monkeys, one potentially crucial area for reach control is the parietal reach region (PRR), in which neurons respond preferentially during reach planning as compared to saccade planning. However, direct causal evidence linking the monkey PRR to the deficits observed in OA is missing. We thus inactivated part of the macaque PRR, in the medial wall of the intraparietal sulcus, and produced the hallmarks of OA, misreaching for peripheral targets but unimpaired saccades. Furthermore, reach errors were larger for the targets preferred by the neural population local to the injection site. These results demonstrate that PRR is causally involved in reach-specific visuomotor pathways, and reach goal disruption in PRR can be a neural basis of OA.

Functional Split between Parietal and Entorhinal Cortices in the Rat

Posterior parietal cortex (PPC) and medial entorhinal cortex (MEC) are important elements of the neural circuit for space, but whether representations in these areas are controlled by the same factors is unknown. We recorded single units simultaneously in PPC and MEC of freely foraging rats and found that a subset of PPC cells are tuned to specific modes of movement irrespective of the animals' location or heading, whereas grid cells in MEC expressed static spatial maps. The behavioral correlates of PPC cells switched completely when the same animals ran in a spatially structured maze or when they ran similar stereotypic sequences in an open arena. Representations in PPC were similar in identical mazes in different rooms where grid cells completely realigned their firing fields. The data suggest that representations in PPC are determined by the organization of actions while cells in MEC are driven by spatial inputs.

Implicit Sensorimotor Mapping of the Peripersonal Space by Gazing and Reaching

Primates often perform coordinated eye and arm movements, contextually fixating and reaching towards nearby objects. This combination of looking and reaching to the same target is used by infants to establish an implicit visuomotor representation of the peripersonal space, useful for both oculomotor and arm motor control. In this work, taking inspiration from such behavior and from primate visuomotor mechanisms, a shared sensorimotor map of the environment, built on a radial basis function framework, is configured and trained by the coordinated control of eye and arm movements. Computational results confirm that the approach seems especially suitable for the problem at hand, and for its implementation on a real humanoid robot. By exploratory gazing and reaching actions, either free or goal-based, the artificial agent learns to perform direct and inverse transformations between stereo vision, oculomotor, and joint-space representations. The integrated sensorimotor map that allows to contextually represent the peripersonal space through different vision and motor parameters is never made explicit, but rather emerges thanks to the interaction of the agent with the environment.

Practice makes perfect, but only with the right hand: Sensitivity to perceptual illusions with awkward grasps decreases with practice in the right but not the left hand

It has been proposed that the visual mechanisms that control well-calibrated actions, such as picking up a small object with a precision grip, are neurally distinct from those that mediate our perception of the object. Thus, grip aperture in such situations has been shown to be remarkably insensitive to many size-contrast illusions. But most of us have practiced such movements hundreds, if not thousands of times. What about less familiar and unpracticed movements? Perhaps they would be less likely to be controlled by specialized visuomotor mechanisms and would therefore be more sensitive to size-contrast illusions. To test this idea, we asked right-handed subjects to pick up small objects using either a normal precision grasp (thumb and index finger) or an awkward grasp (thumb and ring finger), in the context of the Ponzo illusion. Even though this size-contrast illusion had no effect on the scaling of the precision grasp, it did have a significant effect on the scaling of the awkward grasp. Nevertheless, after three consecutive days of practice, even the awkward grasp became resistant to the illusion. In a follow-up experiment, we found that awkward grasps with the left hand (in right handers) did not benefit from practice and remained sensitive to the illusion. We conclude that the skilled target-directed movements are controlled by visual mechanisms that are quite distinct from those controlling unskilled movements, and that these specialized visuomotor mechanisms may be lateralized to the left hemisphere.

Spatial Coincidence of Intentional Actions Modulates an Implicit Visuomotor Control

We investigated a visuomotor mechanism contributing to reach correction: the manual following response (MFR), which is a quick response to background visual motion that frequently occurs as a reafference when the body moves. Although several visual specificities of the MFR have been elucidated, the functional and computational mechanisms of its motor coordination remain unclear mainly because it involves complex relationships among gaze, reaching target, and visual stimuli. To directly explore how these factors interact in the MFR, we assessed the impact of spatial coincidences among gaze, arm reaching, and visual motion on the MFR. When gaze location was displaced from the reaching target with an identical visual motion kept on the retina, the amplitude of the MFR significantly decreased as displacement increased. A factorial manipulation of gaze, reaching-target, and visual motion locations showed that the response decrease is due to the spatial separation between gaze and reaching target but is not due to the spatial separation between visual motion and reaching target. Additionally, elimination of visual motion around the fovea attenuated the MFR. The effects of these spatial coincidences on the MFR are completely different from their effects on the perceptual mislocalization of targets caused by visual motion. Furthermore, we found clear differences between the modulation sensitivities of the MFR and the ocular following response to spatial mismatch between gaze and reaching locations. These results suggest that the MFR modulation observed in our experiment is not due to changes in visual interaction between target and visual motion or to modulation of motion sensitivity in early visual processing. Instead the motor command of the MFR appears to be modulated by the spatial relationship between gaze and reaching.

Practice makes perfect, but only with the right hand: Sensitivity to perceptual illusions with awkward grasps decreases with practice in the right but not the left hand

It has been proposed that the visual mechanisms that control well-calibrated actions, such as picking up a small object with a precision grip, are neurally distinct from those that mediate our perception of the object. Thus, grip aperture in such situations has been shown to be remarkably insensitive to many size-contrast illusions. But most of us have practiced such movements hundreds, if not thousands of times. What about less familiar and unpracticed movements? Perhaps they would be less likely to be controlled by specialized visuomotor mechanisms and would therefore be more sensitive to size-contrast illusions. To test this idea, we asked right-handed subjects to pick up small objects using either a normal precision grasp (thumb and index finger) or an awkward grasp (thumb and ring finger), in the context of the Ponzo illusion. Even though this size-contrast illusion had no effect on the scaling of the precision grasp, it did have a significant effect on the scaling of the awkward grasp. Nevertheless, after three consecutive days of practice, even the awkward grasp became resistant to the illusion. In a follow-up experiment, we found that awkward grasps with the left hand (in right handers) did not benefit from practice and remained sensitive to the illusion. We conclude that the skilled target-directed movements are controlled by visual mechanisms that are quite distinct from those controlling unskilled movements, and that these specialized visuomotor mechanisms may be lateralized to the left hemisphere.

A spiking neural network model of midbrain visuomotor mechanisms that avoids objects by estimating size and distance monocularly

A network of spiking neurons, modeled on the midbrain of fishes, directs a moving animat to avoid large objects and approach small ones. The discrimination is performed by a model of optic tectum that uses monocular vision to extract image size and rate of expansion. Nucleus isthmi which is reciprocally interconnected with tectum, is modeled to estimate object proximity and to scale image size to obtain object size, which if large enough interrupts approach by triggering avoidance.

Methodological issues in measures of imitative reaction times

Ideomotor (IM) theory suggests that observing someone else perform an action activates an internal motor representation of that behaviour within the observer. Evidence supporting the case for an ideomotor theory of imitation has come from studies that show imitative responses to be faster than the same behavioural measures performed in response to spatial cues. In an attempt to replicate these findings, we manipulated the salience of the visual cue and found that we could reverse the advantage of the imitative cue over the spatial cue. We suggest that participants utilised a simple visuomotor mechanism to perform all aspects of this task, with performance being driven by the relative visual salience of the stimuli. Imitation is a more complex motor skill that would constitute an inefficient strategy for rapid performance.

Hemispheric Specialization for the Visual Control of Action Is Independent of Handedness

The idea that visually guided action is independent of visual perception has been supported by neurological, neuropsychological, and behavioral studies. In healthy subjects, evidence for this distinction has come from psychophysical studies of the effects of visual illusions on perceptual judgments and object-directed grasping. This evidence is limited, however, by the fact that virtually all studies have involved right-handed subjects using their dominant hand, which is presumably controlled by the left hemisphere. There is tentative evidence from earlier neurological studies that the left hemisphere may in fact play a special role in the integration of visual and motor information during grasping. We designed two experiments to test this idea. The first experiment involved pictorial illusions, which are known to have robust effects on perceptual judgments but little influence on grasping. Right- and left-handed subjects reached out and grasped objects embedded in two different visual illusions with either their dominant or their nondominant hand. For both right- and left-handed subjects, precision grasping with the left hand, but not with the right, was affected by the illusions. In a follow-up experiment, we examined precision grasping in a more natural setting and showed that left-handed subjects use their nondominant (right) hand significantly more as compared with right-handed subjects. We conclude that visuomotor mechanisms encapsulated in the left hemisphere play a crucial role in the visual control of action and that this hemispheric specialization evolved independently of handedness.