The neuroscience of grasping

People have always been fascinated by the exquisite precision and flexibility of the human hand. When hand meets object, we confront the overlapping worlds of sensorimotor and cognitive functions. We reach for objects, grasp and lift them, manipulate them and use them to act on other objects. This review examines one of these actions--grasping. Recent research in behavioural neuroscience, neuroimaging and electrophysiology has the potential to reveal where in the brain the process of grasping is organized, but has yet to address several questions about the sensorimotor transformations that relate to the control of the hands.     

Evolution of grasping among anthropoids

The prevailing hypothesis about grasping in primates stipulates an evolution from power towards precision grips in hominids. The evolution of grasping is far more complex, as shown by analysis of new morphometric and behavioural data. The latter concern the modes of food grasping in 11 species (one platyrrhine, nine catarrhines and humans). We show that precision grip and thumb-lateral behaviours are linked to carpus and thumb length, whereas power grasping is linked to second and third digit length. No phylogenetic signal was found in the behavioural characters when using squared-change parsimony and phylogenetic eigenvector regression, but such a signal was found in morphometric characters. Our findings shed new light on previously proposed models of the evolution of grasping. Inference models suggest that Australopithecus, Oreopithecus and Proconsul used a precision grip.     

The grasping side of odours

Background

Research on multisensory integration during natural tasks such as reach-to-grasp is still in its infancy. Crossmodal links between vision, proprioception and audition have been identified, but how olfaction contributes to plan and control reach-to-grasp movements has not been decisively shown. We used kinematics to explicitly test the influence of olfactory stimuli on reach-to-grasp movements.

Methodology/Principal Findings

Subjects were requested to reach towards and grasp a small or a large visual target (i.e., precision grip, involving the opposition of index finger and thumb for a small size target and a power grip, involving the flexion of all digits around the object for a large target) in the absence or in the presence of an odour evoking either a small or a large object that if grasped would require a precision grip and a whole hand grasp, respectively. When the type of grasp evoked by the odour did not coincide with that for the visual target, interference effects were evident on the kinematics of hand shaping and the level of synergies amongst fingers decreased. When the visual target and the object evoked by the odour required the same type of grasp, facilitation emerged and the intrinsic relations amongst individual fingers were maintained.

Conclusions/Significance

This study demonstrates that olfactory information contains highly detailed information able to elicit the planning for a reach-to-grasp movement suited to interact with the evoked object. The findings offer a substantial contribution to the current debate about the multisensory nature of the sensorimotor transformations underlying grasping.     

Hallucal grasping behavior in Caluromys (Didelphimorphia: Didelphidae): Implications for primate pedal grasping

A key feature in primate evolution is a foot with a divergent opposable hallucal metatarsal bearing a large peroneal process. Extant primates are characterized by a powerful hallucal grasp—an either “euprimate” or “plesiadapoid-euprimate” ancestor acquisition—that facilitates the exploitation of fine branches, an ability that increased the fitness of ancestral euprimates. In this context, the didelphid marsupial Caluromys has been used as the extant analog to this primate morphotype stage due to some morphological, ecological, and behavioral features. However, the extent to which and the positional and support contexts in which Caluromys uses powerful hallucal grasping are not known. This renders analogies to any mode of “euprimate” or “stem primate” grasping poorly substantiated. The present paper quantifies locomotor and postural behavior, support use, and associated frequencies of hallucal grasping in captive Caluromys philander via analysis of video recordings. During locomotion, Caluromys primarily used diagonal sequence walk, clamber, and climb, whereas stand, foot-hang, and bipedal stand were the dominant postures. Small, fine, horizontal, and moderately inclined branches were frequently used. Overall rates of “apparently powerful hallucal grasps” were high, but were exceptionally high during clamber, climb, foot-hang, and bipedal stand. Additionally, an “apparently powerful hallucal grasp” was very common upon fine, small, steep, and vertical branches. The extensive use of such powerful hallucal grasping provided stability and safety that enabled Caluromys to proficiently utilize fine branches of various orientations. The ability to negotiate such unstable supports, further reflected in foot anatomy, provides evidence that the morphobehavioral complex of Caluromys can serve as an extant analog to the plesiadapoid-euprimate ancestor, represented as a terminal branch feeder with effective hallucal grasping.     

The nature of the primate grasping foot

The grasping primate foot is one of the hallmark adaptations for the order Primates. Prosimian muscle and joint analysis indicates that there are two distinct primate grasping feet. The I–V opposable grasp, in which the hallux opposes the other four digits around a support, is the primitive grasp type utilized by cheirogaleids, lorisides, Daubentonia, and tarsiids. Lemurids and indriids, on the other hand, have a derived I–II adductor grasp, where the grasping action of the hallux and the second digit have been enhanced. This grasp seems to be in response to increasing body size and the use of vertical supports. North American adapids, which were large and possessed the I–V opposable grasp, were probably not able to utilize vertical supports frequently. The recognition of this innovative adaptation, the I–II adductor grasp, which is unique to Madagascar, extends our appreciation of prosimian locomotor capabilities.     

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.     

Evidence of muscle synergies during human grasping

Motor synergies have been investigated since the 1980s as a simplifying representation of motor control by the nervous system. This way of representing finger positional data is in particular useful to represent the kinematics of the human hand. Whereas, so far, the focus has been on kinematic synergies, that is common patterns in the motion of the hand and fingers, we hereby also investigate their force aspects, evaluated through surface electromyography (sEMG). We especially show that force-related motor synergies exist, i.e. that muscle activation during grasping, as described by the sEMG signal, can be grouped synergistically; that these synergies are largely comparable to one another across human subjects notwithstanding the disturbances and inaccuracies typical of sEMG; and that they are physiologically feasible representations of muscular activity during grasping. Potential applications of this work include force control of mechanical hands, especially when many degrees of freedom must be simultaneously controlled.     

Cross-modal interactions between olfaction and vision when grasping

This study used kinematics to investigate the integration between vision and olfaction during grasping movements. Participants were requested to smell an odorant and then grasp an object presented in central vision. The results indicate that if the target was small (e.g., a strawberry), the time and amplitude of maximum hand aperture were later and greater, respectively, when the odor evoked a larger object (e.g., an orange) than when the odor evoked an object of a similar size as the target or no odor was presented. Conversely, the time and amplitude of maximum hand aperture were earlier and reduced, respectively, when the target was large (e.g., a peach) and the odor evoked a smaller sized object (e.g., an almond) than when the odor evoked an object of a similar size as the target or no odor was presented. Taken together, these results support the evidence of cross-modal links between olfaction and vision and extend this notion to goal-directed actions.     

Design of grasping methodologies for rotational assembly components

This article describes a design methodology for grasping assembly components. Three heuristics are developed. The first determines feasible grasping configurations based on component geometric information. The second heuristic determines feasible grasping configurations by including gripper functional attributes. The third heuristic generates the final set of grasping configurations by including the area available for grasping a component. An interactive program written in Fortran 77 is developed to capture the user inputs, and a sample application is described. The methodology does not assume an initial feeding state of the component to the robot. The grasping configurations generated (if more than one) provide the designer with alternate feasible feeding methods.     

Sensory-motor coordination during grasping and manipulative actions.

Goal-directed grasping and manipulation of objects are human skills that depend on automatic sensory control in which predictive feed-forward mechanisms integrate somatosensory and visual signals with sensory-motor memory systems. Memory representations of physical and task-relevant properties of the object play a pivotal role. Anticipatory strategies are crucial when purposeful actions arise from learned relationships between afferent patterns and efferent commands. The development of even elementary precision grip skills is a protracted process not concluded until early adolescence. Not surprisingly, the neural control of manual actions engages most central nervous system areas known to be involved in motor control.     

Interactions between areas of the cortical grasping network

Skilled grasp is a sensorimotor process requiring the brain to extract sensory cues from the environment to shape a motor command. Although a large body of literature has focused on which brain areas either integrate the visual object's properties or control the motor output, it is still unclear how grasp-related information is transferred from one area to another. Understanding interactions between brain areas is crucial for the study of visuomotor transformations. Recently, new advances in both human and non-human primates have shown it is possible to study cortico-cortical interactions during different task contexts. This sheds new light on how brain areas are integrated in a dynamic network for controlling grasping actions.     

Tangential finger forces use mechanical advantage during static grasping

When grasping and manipulating objects, the central controller utilizes the mechanical advantage of the normal forces of the fingers for torque production. Whether the same is valid for tangential forces is unknown. The main purpose of this study was to determine the patterns of finger tangential forces and the use of mechanical advantage as a control mechanism when dealing with objects of nonuniform finger positioning. A complementary goal was to explore the interaction of mechanical advantage (moment arm) and the role a finger has as a torque agonist/antagonist with respect to external torques (±0.4 N m). Five 6-df force/torque transducers measured finger forces while subjects held a prism handle (6 cm width × 9 cm height) with and without a single finger displaced 2 cm (handle width). The effect of increasing the tangential moment arm was significant (p < .01) for increasing tangential forces (in >70% of trials) and hence creating greater moments. Thus, the data provides evidence that the grasping system as a rule utilizes mechanical advantage for generating tangential forces. The increase in tangential force was independent of whether the finger was acting as a torque agonist or antagonist, revealing their effects to be additive.     

Both reaching and grasping are impacted by temporarily induced paresthesia

Abstract

Along with visual feedback, somatosensory feedback provides the nervous system with information regarding movement performance. Somatosensory system damage disrupts the normal feedback process, which can lead to a pins and needles sensation, or paresthaesia, and impaired movement control. The present study assessed the impact of temporarily induced median nerve paresthaesia, in individuals with otherwise intact sensorimotor function, on goal-directed reaching and grasping movements. Healthy, right-handed participants performed reach and grasp movements to five wooden Efron shapes, of which three were selected for analysis. Participants performed the task without online visual feedback and in two somatosensory conditions: 1) normal; and 2) disrupted somatosensory feedback. Disrupted somatosensory feedback was induced temporarily using a Digitimer (DS7AH) constant current stimulator. Participants’ movements to shapes 15 or 30?cm to the right of the hand’s start position were recorded using a 3?D motion analysis system at 300?Hz (Optotrak 3?D Investigator). Analyses revealed no significant differences for reaction time. Main effects for paresthaesia were observed for temporal and spatial aspects of the both the reach and grasp components of the movements. Although participants scaled their grip aperture to shape size under paresthaesia, the movements were smaller and more variable. Overall participants behaved as though they perceived they were performing larger and faster movements than they actually were. We suggest the presence of temporally induced paresthaesia affected online control by disrupting somatosensory feedback of the reach and grasp movements, ultimately leading to smaller forces and fewer corrective movements.     

Modeling the time-dependent effect of the Ebbinghaus illusion on grasping

Various authors have reported a small but consistent effect of the Ebbinghaus illusion on the maximum opening of the hand during prehension. This effect has been interpreted in various ways. In the present study, we focus on the time-course of the effect of contextual elements on grasping. The analysis presented here is based on a model for the control of the digits that uses two movement parameters (the approach parameter and the intended contact positions). These two parameters are based on different spatial attributes (flanker-target distance and target-edge position). As we assume that the perception of both attributes is veridical, there is no need for on-line corrections in the model. We show that this model predicts all time-dependent effects of the Ebbinghaus display on grasping. Human behavior can show a reduction in context effects over time without assuming an underlying shift from illusory towards veridical size information.     

On the analysis of hand synergies during grasping in weightlessness

The aim of this paper was to analyse how the strategies implemented by the Central Nervous System to control the hand during grasping are modified under microgravity conditions. Two right-handed subjects carried out simple grasping tasks during parabolic flights. The trajectories of the fingers of the hand were recorded using a sensorised glove and processed in order to extract a variable (here indicated as K) which can indicated the degree of synergies existing among the fingers. The results showed that K was quite small during the trial at 1g while becoming significantly greater than 1 during the first parabolas. Then, the value k decreased to the values at 1 g after some parabolas. These results suggested a possible adaptation process of the manipulation abilities during the permanence at 0g conditions. Future extensive trials will be performed in order to confirm these preliminary results.     

Prehension synergies during nonvertical grasping,I: experimental observations

The mechanical complexities of rotating an object through the gravity field present a formidable challenge to the human central nervous system (CNS). The current study documents the finger force patterns selected by the CNS when performing one-, two-, and four-finger grasping while holding an object statically at various orientations with respect to vertical. Numerous mechanically unnecessary behaviors were observed. These included: nonzero tangential forces for horizontal handle orientations, large internal forces (i.e., those in excess of equilibrium requirements) for all orientations, and safety margins between 50 and 90%. Additionally, none of the investigated measures were constant across orientations or could be represented as a simple trigonometric function of orientation. Nonetheless, all measures varied in systematic (and sometimes symmetric) ways with orientation. The results suggest that the CNS selects force patterns that are based on mechanical principles but also that are not simply related to object orientation. This study is complemented by a second paper that provides an in-depth analysis of the mechanics of nonvertical grasping and accounts for many of the observed results with numerical optimization (see Part II – current issue). Together, the papers demonstrate that the CNS is likely to utilize optimization processes when controlling prehensile actions.Supported in part by NIH grants AR-48563, AG-018751 and NS-35032.     

Precision grasping in humans: from motor control to cognition

In the past decade, functional neuroimaging has proved extremely useful in mapping the human motor circuits involved in skilled hand movements. However, one major drawback of this approach is the impossibility to determine the exact contribution of each individual cortical area to precision grasping. Because transcranial magnetic stimulation (TMS) makes it possible to induce a transient 'virtual' lesion of discrete brain regions in healthy subjects, it has been extensively used to provide direct insight into the causal role of a given area in human motor behaviour. Recent TMS studies have allowed us to determine the specific contribution, as well as the timing and the hemispheric lateralisation, of distinct parietal and frontal areas to the control of both the kinematics and dynamics of precision grasping. Moreover, recent researches have shown that the same cortical network may contribute to language and number processing, supporting the existence of tight interactions between processes involved in cognition and actions. The aim of this paper is to offer a concise overview of recent studies that have investigated the neural correlates of precision grasping and the possible contribution of the motor system to higher cognitive functions such as language and number processing.     

Stiffness map of the grasping contact areas of the human hand

The elasticity and damping of the soft tissues of the hand contribute to dexterity while grasping and also help to stabilise the objects in manipulation tasks. Although some previous works have studied the force-displacement response of the fingertips, the responses in all other regions of the hand that usually participate in grasping have not been analysed to date. In this work we performed experimental measurements in 20 subjects to obtain a stiffness map of the different grasping contact areas of the human hand. A force-displacement apparatus was used to simultaneously measure force and displacement at 39 different points on the hand at six levels of force ranging from 1 N to 6 N. A non-linear force-displacement response was found for all points, with stiffness increasing with the amount of force applied. Mean stiffness for the different points and force levels was within the range from 0.2 N/mm to 7.7 N/mm. However, the stiffness range and variation with level of force were found to be different from point to point. A total of 13 regions with similar stiffness behaviours were identified. The stiffness in the fingertips increased linearly with the amount of force applied, while in the palm it remained more constant for the range of forces considered. It is hypothesised that the differences in the stiffness behaviour from one region to another allow these regions to play different roles during grasping.