Differential cortical activity for precision and whole-hand visually guided grasping in humans

Effective grasping involves the remarkable ability to implement multiple grasp configurations such as precision grip (PG; opposition between the index finger and thumb) and whole-hand grasp (WHG), depending on the properties of the object grasped (e.g. size, shape and weight). In the monkey brain, different groups of cells in the anterior-lateral bank of the intraparietal sulcus (area AIP) are differentially active for various hand configurations during grasping of differently shaped objects. Visually guided grasping studies in humans suggest the anterior intraparietal sulcus (aIPS) as the homologue of macaque area AIP, but leave unresolved the question of whether activity in human aIPS reflects the relationship between object size and grasp configuration, as in macaques. To address this issue, a human fMRI study was conducted in which objects were grasped with the right hand while object size was varied. The results indicated that the left aIPS was active when the subjects naturally adopted a PG to grasp the small object but showed a much weaker response when subjects naturally adopted a WHG to grasp the large object. The primary motor cortex and somatosensory cortices were active for both PG and WHG. Our results suggest that, in humans, the aIPS is centrally involved in determining the type of grasp.     

Human parietal and primary motor cortical interactions are selectively modulated during the transport and grip formation of goal-directed hand actions

Posterior parietal cortex (PPC) constitutes a critical cortical node in the sensorimotor system in which goal-directed actions are computed. This information then must be transferred into commands suitable for hand movements to the primary motor cortex (M1). Complexity arises because reach-to-grasp actions not only require directing the hand towards the object (transport component), but also preshaping the hand according to the features of the object (grip component). Yet, the functional influence that specific PPC regions exert over ipsilateral M1 during the planning of different hand movements remains unclear in humans. Here we manipulated transport and grip components of goal-directed hand movements and exploited paired-pulse transcranial magnetic stimulation (_ppTMS) to probe the functional interactions between M1 and two different PPC regions, namely superior parieto-occipital cortex (SPOC) and the anterior region of the intraparietal sulcus (aIPS), in the left hemisphere. We show that when the extension of the arm is required to contact a target object, SPOC selectively facilitates motor evoked potentials, suggesting that SPOC-M1 interactions are functionally specific to arm transport. In contrast, a different pathway, linking the aIPS and ipsilateral M1, shows enhanced functional connections during the sensorimotor planning of grip. These results support recent human neuroimaging findings arguing for specialized human parietal regions for the planning of arm transport and hand grip during goal-directed actions. Importantly, they provide new insight into the causal influences these different parietal regions exert over ipsilateral motor cortex for specific types of planned hand movements.     

Cortical dynamics of sensorimotor integration during grasp planning

Our sensorimotor interactions with objects are guided by their current spatial and perceptual features, as well as by learned object knowledge. A fresh red tomato is grasped differently than a soft overripe tomato, even when those objects possess the same spatial metrics of size and shape. Objects' spatial and perceptual features need to be integrated during grasping, but those features are analyzed in two anatomically distinct neural pathways. The anterior intraparietal sulcus (aIPS) might support the integration of those features. We combine transcranial magnetic stimulation (TMS) interference, EEG recordings, and psychophysical methods to test aIPS causal contributions to sensorimotor integration, characterizing the dynamics of those contributions during motor planning. Human subjects performing grasping movements were provided with visual information about a target object, namely spatial and pictorial cues, whose availability and information value were independently modulated on each trial. Maximally informative visual cues, irrespective of their spatial or perceptual nature, led to enhanced motor preparatory activity early during movement planning, and to stronger spatial congruency between finger trajectories and target object. Disturbing aIPS activity with single-pulse TMS within 200 ms after object presentation reduced those electrophysiological and behavioral indices of enhanced motor planning. TMS interference with aIPS also disturbed subjects' ability to use learned object knowledge during motor planning. These results indicate that aIPS is necessary for the fast generation of a new motor plan on the basis of both spatial and pictorial cues. Furthermore, as learned object knowledge becomes available, aIPS comes to strongly depend on this prior information for structuring the motor plan.     

Continuous theta-burst stimulation over the dorsal premotor cortex interferes with associative learning during object lifting

When lifting objects of different mass, humans scale grip force according to the expected mass. In this context, humans are able to associate a sensory cue, such as a colour, to a particular mass of an object and link this association to the grip forces necessary for lifting. Here, we study the role of the dorsal premotor cortex (PMd) in setting-up an association between a colour cue and a particular mass to be lifted. Healthy right-handed subjects used a precision grip between the index finger and thumb to lift two different masses. Colour cues provided information about which of the two masses subjects would have to lift. Subjects first performed a series of lifts with the right hand to establish a stable association between a colour cue and a mass, followed by 20 sec of continuous high frequency repetitive trancranial magnetic stimulation using a recently developed protocol (continuous theta-burst stimulation, cTBS) over (i) the left primary motor cortex, (ii) the left PMd and (iii) the left occipital cortex to be commenced by another series of lifts with either the right or left hand. cTBS over the PMd, but not over the primary motor cortex or O1, disrupted the predictive scaling of isometric finger forces based on colour cues, irrespective of whether the right or left hand performed the lifts after the stimulation. Our data highlight the role of the PMd to generalize and maintain associative memory processes relevant for predictive control of grip forces during object manipulation.     

Finger pressure adjustments to various object configurations during precision grip in humans and monkeys

In this study, we recorded the pressure exerted onto an object by the index finger and the thumb of the preferred hand of 18 human subjects and either hand of two macaque monkeys during a precision grasping task. The to‐be‐grasped object was a custom‐made device composed by two plates which could be variably oriented by a motorized system while keeping constant the size and thus grip dimension. The to‐be‐grasped plates were covered by an array of capacitive sensors to measure specific features of finger adaptation, namely pressure intensity and centroid location and displacement. Kinematic measurements demonstrated that for human subjects and for monkeys, different plate configurations did not affect wrist velocity and grip aperture during the reaching phase. Consistently, at the instant of fingers‐plates contact, pressure centroids were clustered around the same point for all handle configurations. However, small pressure centroid displacements were specifically adopted for each configuration, indicating that both humans and monkeys can display finger adaptation during precision grip. Moreover, humans applied stronger thumb pressure intensity, performed less centroid displacement and required reduced adjustment time, as compared to monkeys. These pressure patterns remain similar when different load forces were required to pull the handle, as ascertained by additional measurements in humans. The present findings indicate that, although humans and monkeys share common features in motor control of grasping, they differ in the adjustment of fingertip pressure, probably because of skill and/or morphology divergences. Such a precision grip device may form the groundwork for future studies on prehension mechanisms.     

How do object size and rigidity affect reaching and grasping in infants with Down syndrome?

Reaching and grasping skills have been described to emerge from a dynamic interaction between intrinsic and extrinsic factors. The purpose of the present study was to investigate the interaction between such an intrinsic factor, Down syndrome, and extrinsic factors, such as different object properties. Seven infants with Down syndrome and seven infants with typical development were assessed at the ages of 4, 5 and 6 months. The findings showed that object size influenced the kinematics of reaching for the infants with Down syndrome and the grasping frequency for the typical infants. The object rigidity was shown to have a major influence on grasping frequency.     

Weight-specific anticipatory coding of grip force in human dorsal premotor cortex

The dorsal premotor cortex (PMd) uses prior sensory information for motor preparation. Here, we used a conditioning-and-map approach in 11 healthy male humans (mean age 27 years) to further clarify the role of PMd in anticipatory motor control. We transiently disrupted neuronal processing in PMd, using either continuous theta burst stimulation (cTBS) at 80% (inhibitory cTBS) or 30% (sham cTBS) of active motor threshold. The conditioning effects of cTBS on preparatory brain activity were assessed with functional MRI, while participants lifted a light or heavy weight in response to a go-cue (S2). An additional pre-cue (S1) correctly predicted the weight in 75% of the trials. Participants were asked to use this prior information to prepare for the lift. In the sham condition, grip force showed a consistent undershoot, if the S1 incorrectly prompted the preparation of a light lift. Likewise, an S1 that falsely announced a heavy weight produced a consistent overshoot in grip force. In trials with incorrect S1, preparatory activity in left PMd during the S1-S2 delay period predicted grip force undershoot but not overshoot. Real cTBS selectively abolished this undershoot in grip force. Furthermore, preparatory S1-S2 activity in left PMd no longer predicted the individual undershoot after real cTBS. Our results provide converging evidence for a causal involvement of PMd in anticipatory downscaling but not upscaling of grip force, suggesting an inhibitory role of PMd in anticipatory grip force control during object lifting.     

The effects of digital anaesthesia on predictive grip force adjustments during vertical movements of a grasped object

Grip force adjustments to fluctuations of inertial loads induced by vertical arm movements with a grasped object were analysed during normal and impaired finger sensibility. Normally grip force is modulated in a highly economical way in parallel with fluctuations of load force. Two subjects performed vertical up and down movements of a grasped object, both with normal finger sensibility and then cutaneously anaesthetized finger sensibility. Short breaks were taken in between single movements, during which the object was held stationary. After digital anaesthesia was applied to the grasping fingers, both subjects substantially increased the grip force. The grip force amplitude and timing still anticipated changes in load force, although the established grip force had already overcome movement-induced load force peaks. This implies that the increase of grip force and consequently the elevated force ratio between maximum grip and maximum load force are not processed to alter the feedforward system of grip force control. Cutaneous afferent information from the grasping digits appears to be necessary for economic scaling of the grip force level, but it plays a subordinate role in the precise anticipatory temporal coupling of grip and load forces during voluntary object manipulation.     

The continuous updating of grasp in response to dynamic changes in object size, hand size and distractor proximity

Reaching out to pick up an object seems a trivial matter, but selecting the appropriate hand configuration requires a series of complex computations that process the object's dimensions, orientation and environment. A current debate in motor control concerns how and when the motor system responds to unexpected changes in the visual and spatial properties of objects to be grasped. In the current experiment, visual manipulations that increased either target size, distractor proximity or hand size were applied gradually and continuously throughout reach to grasp movements. All manipulations were associated with early and continuous modifications of the grasping component, but only an increase in hand size affected transport characteristics. This suggests that visual information of both the object and the effector are continuously processed in movement computations, in keeping with models of motor control that posit high weighting for online sensory feedback.     

Grip force behavior during object manipulation in neurological disorders: toward an objective evaluation of manual performance deficits.

The control of prehensile finger forces is an essential feature of skilled manual performance. The basic aspects of healthy grip force behavior have been well documented. In healthy subjects, grip force is precisely adjusted to the mechanical object properties. Grip force is always slightly higher than the minimum necessary to prevent the object from slipping. When we move a hand-held object, grip force is modulated in parallel with movements-induced load fluctuations without an obvious delay. The absence of a temporal delay between grip and load force profiles suggests that the central nervous system is able to predict the load variations before the intended manipulation and consequently regulates grip force in anticipation. Feedback from the grasping fingertips is used to adjust the level of applied fingertip force efficiently to the actual loading requirements. Pathologic grip force control affects the efficiency of produced force and the precision of the temporal coupling between grip and load force profiles. Here, we review the characteristics of pathologic grip force behavior in various neurological disorders. Detailed examination of grip force control is simple and well suited for the objective evaluation of impaired motor function of the hand and its rehabilitation.     

Moving objects with clumsy fingers: how predictive is grip force control in patients with impaired manual sensibility?

OBJECTIVE: Anticipatory grip force adjustments to movement-induced load fluctuations of a hand-held object suggest that motion planning is based on an internal forward model of both the external object properties and the dynamics of the own motor apparatus. However, the central nervous system also refers to real time sensory feedback from the grasping digits in order to achieve a highly economical coupling between grip force and the actual loading requirements. METHODS: We analyzed grip force control during vertical point-to-point arm movements with a hand-held instrumented object in 9 patients with moderately impaired tactile sensibility of the grasping digits due to chronic median nerve compression (n = 3), axonal (n = 3) and demyelinating sensory polyneuropathy (n = 3) in comparison to 9 healthy age- and sex-matched control subjects. Point-to-point arm movements started and ended with the object being held stationary at rest. Load force changes arose from inertial loads related to the movement. A maximum of load force occurred early in upward and near the end of downward movements. RESULTS: Compared to healthy controls, patients with impaired manual sensibility generated similar static grip forces during stationary holding of the object and similar force ratios between maximum grip and load force. These findings reflect effective grip force scaling in relation to the movement-induced loads despite reduced afferent feedback from the grasping digits. For both groups the maxima of grip and load force coincided very closely in time, indicating that the temporal regulation of the grip force profile with the load profile was processed with a similar high precision. In addition, linear regression analyses between grip and load forces during movement-related load increase and load decrease phases revealed a similar precise temporo-spatial coupling between grip and load forces for patients and controls. CONCLUSIONS: Our results suggest that the precise and anticipatory adjustment of the grip force profile to the load force profile arising from voluntary arm movements with a hand-held object is centrally mediated and less under sensory feedback control. As suggested by previous investigations, the efficient scaling of the grip force magnitude in relation to the movement-induced loads may be intact when deficits of tactile sensibility from the grasping fingers are moderate.     

Force requirements of observed object lifting are encoded by the observer’s motor system: a TMS study

Several transcranial magnetic stimulation (TMS) studies have reported facilitation of the primary motor cortex (M1) during the mere observation of actions. This facilitation was shown to be highly congruent, in terms of somatotopy, with the observed action, even at the level of single muscles. With the present study, we investigated whether this muscle‐specific facilitation of the observer’s motor system reflects the degree of muscular force that is exerted in an observed action. Two separate TMS experiments are reported in which corticospinal excitability was measured in the hand area of M1 while subjects observed the lifting of objects of different weights. The type of action ‘grasping‐and‐lifting‐the‐object’ was always identical, but the grip force varied according to the object’s weight. In accordance to previous findings, excitability of M1 was shown to modulate in a muscle‐specific way, such that only the cortical representation areas in M1 that control the specific muscles used in the observed lifting action became increasingly facilitated. Moreover, muscle‐specific M1 facilitation was shown to modulate to the force requirements of the observed actions, such that M1 excitability was considerably higher when observing heavy object lifting compared with light object lifting. Overall, these results indicate that different levels of observed grip force are mirrored onto the observer’s motor system in a highly muscle‐specific manner. The measured force‐dependent modulations of corticospinal excitability in M1 are hypothesized to be functionally relevant for scaling the observed grip force in the observer’s own motor system. In turn, this mechanism may contribute, at least partly, to the observer’s ability to infer the weight of the lifted object.     

Relative size of numerical magnitude induces a size-contrast effect on the grip scaling of reach-to-grasp movements

Previous research found that quantitative information labelled on target objects of grasping movement modulates grip apertures. While the interaction between numerical cognition and sensorimotor control may reflect a general representation of magnitude underpinned by the parietal cortex, the nature of this embodied cognitive processing remains unclear. In the present study, we examined whether the numerical effects on grip aperture can be flexibly modulated by the relative magnitude between numbers under a context, which suggests a trial-by-trial comparison mechanism to underlie this effect. The participants performed visual open-loop grasping towards one of two adjacent objects that were of the same physical size but labelled with different Arabic digits. Analysis of participants' grip apertures revealed a numerical size-contrast effect, in which the same numerical label (i.e., 5) led to larger grip apertures when it was accompanied by a smaller number (i.e., 2) than by a larger number (i.e., 8). The corrected grip aperture over the time course of movement showed that the numerical size-contrast effect remained significant throughout the grasping movement, despite a trend of gradual dissipation. Our findings demonstrated that interactions between number and action critically depend on the size-contrast of magnitude information in the context. Such a size-contrast effect might result from a general system, which is sensitive to relative magnitude, for different quantity domains. Alternatively, the magnitude representations of numbers and action might be processed separately and interact at a later stage of motor programming.     

Effects of carpal tunnel syndrome on adaptation of multi-digit forces to object texture

Objective

The ability to adapt digit forces to object properties requires both anticipatory and feedback-driven control mechanisms which can be disrupted in individuals with a compromised sensorimotor system. Carpal tunnel syndrome (CTS) is a median nerve compression neuropathy affecting sensory and motor function in a subset of digits in the hand. Our objective was to examine how CTS patients coordinate anticipatory and feedback-driven control for multi-digit grip force adaptation.

Methods

We asked CTS patients and healthy controls to grasp, lift, and hold an object with different textures.

Results

CTS patients effectively adapted their digit forces to changes in object texture, but produced excessive grip forces. CTS patients also produced larger peak force rate profiles with fewer modulations of normal force prior to lift onset than did controls and continued to increase grip force throughout the lift whereas forces were set at lift onset for the controls.

Conclusions

These findings suggest that CTS patients use less online sensory feedback for fine-tuning their grip forces, relying more on anticipatory control than do healthy controls.

Significance

These characteristics in force adaptation in CTS patients indicate impaired sensorimotor control which leads to excessive grip forces with the potential to further exacerbate their median nerve compression.     

Rostrocaudal functional gradient among the pre‐dorsal premotor cortex,dorsal premotor cortex and primary motor cortex in goal‐directed motor behaviour

The dorsal premotor cortex residing in the dorsolateral aspect of area 6 is a rostrocaudally elongated area that is rostral to the primary motor cortex (M1) and caudal to the prefrontal cortex. This region, which is subdivided into rostral [pre‐dorsal premotor cortex (pre‐PMd)] and caudal [dorsal premotor cortex proper (PMd)] components, probably plays a central role in planning and executing actions to achieve a behavioural goal. In the present study, we investigated the functional specializations of the pre‐PMd, PMd, and M1, because the synthesis of the specific functions performed by each area is considered to be essential. Neurons were recorded while monkeys performed a conditional visuo‐goal task designed to include separate processes for determining a behavioural goal (reaching towards a right or left potential target) on the basis of visual object instructions, specifying actions (direction of reaching) to be performed on the basis of the goal, and preparing and executing the action. Neurons in the pre‐PMd and PMd retrieved and maintained behavioural goals without encoding the visual features of the visual object instructions, and subsequently specified the actions by multiplexing the goals with the locations of the targets. Furthermore, PMd and M1 neurons played a major role in representing the action during movement preparation and execution, whereas the contribution of the pre‐PMd progressively decreased as the time of the actual execution of the movement approached. These findings revealed that the multiple processing stages necessary for the realization of an action to accomplish a goal were implemented in an area‐specific manner across a functional gradient from the pre‐PMd to M1 that included the PMd as an intermediary.     

A neural network simulating human reach-grasp coordination by continuous updating of vector positioning commands.

We developed a neural network model to simulate temporal coordination of human reaching and grasping under variable initial grip apertures and perturbations of object size and object location/orientation. The proposed model computes reach-grasp trajectories by continuously updating vector positioning commands. The model hypotheses are (1) hand/wrist transport, grip aperture, and hand orientation control modules are coupled by a gating signal that fosters synchronous completion of the three sub-goals. (2) Coupling from transport and orientation velocities to aperture control causes maximum grip apertures that scale with these velocities and exceed object size. (3) Part of the aperture trajectory is attributable to an aperture-reducing passive biomechanical effect that is stronger for larger apertures. (4) Discrepancies between internal representations of targets partially inhibit the gating signal, leading to movement time increases that compensate for perturbations. Simulations of the model replicate key features of human reach-grasp kinematics observed under three experimental protocols. Our results indicate that no precomputation of component movement times is necessary for online temporal coordination of the components of reaching and grasping.     

Impaired grip force modulation in the ipsilesional hand after unilateral middle cerebral artery stroke

Understanding grasping control after stroke is important for relearning motor skills. The authors examined 10 individuals (5 males; 5 females; ages 32-86) with chronic unilateral middle cerebral artery (MCA) stroke (4 right lesions; 6 left lesions) when lifting a novel test object using skilled precision grip with their ipsilesional ("unaffected") hand compared to healthy controls (n = 14; 6 males; 8 females; ages 19-86). All subjects possessed normal range of motion, cutaneous sensation, and proprioception in the hand tested and had no apraxia or cognitive deficits. Subjects lifted the object 10 times at each object weight (260 g, 500 g, 780 g) using a moderately paced self-selected lifting speed. The normal horizontal ("grip") force and vertical tangential ("lift") force were separately measured at the thumb and index finger. Regardless of the object weight or stroke location, the stroke group generated greater grip forces at liftoff of the object (> or =39%; P < or = 0.05) and across the dynamic (P < or = 0.05) and static portions (P < or = 0.05) of the lifts compared to the healthy group. Peak lift forces were equivalent between groups, suggesting accurate load force information processing occurred. These results warrant further investigation of altered sensorimotor processing or compensatory biomechanical strategies that may lead to inaccurate grip force execution after strokes.     

Objective assessment of progression in Huntington's disease: a 3-year follow-up study

Objective measures to assess progression of Huntington's disease (HD) are desirable. The authors have previously found that patients with HD with higher Unified Huntington's Disease Rating Scale (UHDRS) motor scores exhibited higher variability of isometric grip forces while grasping an object. Therefore, the authors assessed grip force variability during this task in 10 HD patients with a 3-year follow-up. Grip force variability increased in all patients at the follow-up. Thus, grip force variability during grasping might be an objective and quantitative measure to assess motor deficits associated with the progression of HD.     

Grip-dependent cortico-spinal excitability during grasping imagination and execution

Studies converge in indicating a substantial similarity of the rules and mechanisms underlying execution, observation and imagery of actions, along with a large overlapping of their neural substrates. Recent transcranial magnetic stimulation (TMS) studies have demonstrated a muscle-specific facilitation of the observer's motor system for force requirement and type of grip during grasping observation. However, whether similar fine-tuned muscle-specificity occurs even during imagination, when subjects are free to select the most convenient grip configuration, is still unknown. Here we applied TMS over the primary motor cortex and measured the corticospinal excitability (MEP) in three muscles (FDI, ADM and FDS) while subjects imagined grasping spheres of different dimensions and materials. This range of object weights and sizes (diameters) allowed subjects to freely imagine the most suitable grip configuration among several possibilities. Activation measured during grasping imagination has been also compared to that obtained during real execution (EMG recorded from the same muscles).We found that during imagination of grasping small objects, the FDI muscle was more active than the ADM and the FDS, whereas the opposite pattern was found for big objects. Imagination of medium size objects, instead, required an equal involvement of the three muscles. The same pattern was observed when subjects were asked to perform the action. This suggests that during imagination, the cortico-spinal system is modulated in a muscle-specific/grip-specific way, as if the action would be really performed. However, when force was required (i.e., for the aluminum objects), the motor activation obtained during action execution was more fine-tuned to object dimensions than the facilitation recorded during imagination, suggesting a separate control of force production.