Adaptation and compensation for somatosensory deficits in object handling: evidence from a patient with large fibre sensory neuropathy

The purpose of this study was to determine the contributions of feedforward and feedback processes on grip force regulation and object orientation during functional manipulation tasks. One patient with massive somatosensory loss resulting from large fibre sensory neuropathy, and ten control participants were recruited. Three experiments were conducted: 1) perturbation to static holding; 2) discrete vertical movement; and 3) functional grasp and place. The availability of visual feedback was also manipulated to assess the nature of compensatory mechanisms. Results from experiment 1 indicated that both the deafferented patient and controls used anticipatory grip force adjustments prior to self-induced perturbation to static holding. The patient exhibited increased grip response time, but the magnitude of grip force adjustments remained correlated with perturbation forces in the self-induced and external perturbation conditions. In experiment 2, the patient applied peak grip force substantially in advance of maximum load force. Unlike controls, the patient's ability to regulate object orientation was impaired without visual feedback. In experiment 3, the duration of unloading, transport and release phases were longer for the patient, with increased deviation of object orientation at phase transitions. These findings show that the deafferented patient uses distinct modes of anticipatory control according to task constraints, and that responses to perturbations are mediated by alternative afferent information. The loss of somatosensory feedback thus appears to impair control of object orientation, while variation in the temporal organization of functional tasks may reflect strategies to mitigate object instability associated with changes in movement dynamics.

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Grip Force-Load Force Coupling Is Influenced by Altered Visual Feedback about Object Kinematics

Journal of Motor Behavior ◽

10.1080/00222895.2019.1664977 ◽

2019 ◽

Vol 52 (5) ◽

pp. 612-624 ◽

Cited By ~ 1

Author(s):

Francis M. Grover ◽

Sarah M. Schwab ◽

Michael A. Riley

Keyword(s):

Visual Feedback ◽

Grip Force ◽

Load Force ◽

Force Load ◽

Force Coupling

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Delayed Visual Feedback Affects Both Manual Tracking and Grip Force Control When Transporting a Handheld Object

Journal of Neurophysiology ◽

10.1152/jn.00174.2010 ◽

2010 ◽

Vol 104 (2) ◽

pp. 641-653 ◽

Cited By ~ 36

Author(s):

Fabrice R. Sarlegna ◽

Gabriel Baud-Bovy ◽

Frédéric Danion

Keyword(s):

Visual Feedback ◽

Grip Force ◽

Task Complexity ◽

Dynamic Properties ◽

Internal Representation ◽

Object Motion ◽

Load Force ◽

Manual Tracking ◽

Actual Object ◽

Delayed Visual Feedback

When we manipulate an object, grip force is adjusted in anticipation of the mechanical consequences of hand motion (i.e., load force) to prevent the object from slipping. This predictive behavior is assumed to rely on an internal representation of the object dynamic properties, which would be elaborated via visual information before the object is grasped and via somatosensory feedback once the object is grasped. Here we examined this view by investigating the effect of delayed visual feedback during dextrous object manipulation. Adult participants manually tracked a sinusoidal target by oscillating a handheld object whose current position was displayed as a cursor on a screen along with the visual target. A delay was introduced between actual object displacement and cursor motion. This delay was linearly increased (from 0 to 300 ms) and decreased within 2-min trials. As previously reported, delayed visual feedback altered performance in manual tracking. Importantly, although the physical properties of the object remained unchanged, delayed visual feedback altered the timing of grip force relative to load force by about 50 ms. Additional experiments showed that this effect was not due to task complexity nor to manual tracking. A model inspired by the behavior of mass-spring systems suggests that delayed visual feedback may have biased the representation of object dynamics. Overall, our findings support the idea that visual feedback of object motion can influence the predictive control of grip force even when the object is grasped.

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Effects of local and core body temperature on grip force modulation during movement-induced load force fluctuations

European Journal of Applied Physiology ◽

10.1007/s00421-008-0671-4 ◽

2008 ◽

Vol 103 (1) ◽

pp. 59-69 ◽

Cited By ~ 18

Author(s):

Stephen S. Cheung ◽

Luke F. Reynolds ◽

Mark A. B. Macdonald ◽

Constance L. Tweedie ◽

Robin L. Urquhart ◽

...

Keyword(s):

Body Temperature ◽

Grip Force ◽

Core Body Temperature ◽

Load Force ◽

Force Fluctuations ◽

Force Modulation ◽

Core Body

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Intermittent Visuomotor Processing in the Human Cerebellum, Parietal Cortex, and Premotor Cortex

Journal of Neurophysiology ◽

10.1152/jn.00718.2005 ◽

2006 ◽

Vol 95 (2) ◽

pp. 922-931 ◽

Cited By ~ 65

Author(s):

David E. Vaillancourt ◽

Mary A. Mayka ◽

Daniel M. Corcos

Keyword(s):

Parietal Cortex ◽

Visual Feedback ◽

Visual Information ◽

Grip Force ◽

Premotor Cortex ◽

Force Variability ◽

Neural Activation ◽

Control Force ◽

Force Condition ◽

Visuomotor Processing

The cerebellum, parietal cortex, and premotor cortex are integral to visuomotor processing. The parameters of visual information that modulate their role in visuomotor control are less clear. From motor psychophysics, the relation between the frequency of visual feedback and force variability has been identified as nonlinear. Thus we hypothesized that visual feedback frequency will differentially modulate the neural activation in the cerebellum, parietal cortex, and premotor cortex related to visuomotor processing. We used functional magnetic resonance imaging at 3 Tesla to examine visually guided grip force control under frequent and infrequent visual feedback conditions. Control conditions with intermittent visual feedback alone and a control force condition without visual feedback were examined. As expected, force variability was reduced in the frequent compared with the infrequent condition. Three novel findings were identified. First, infrequent (0.4 Hz) visual feedback did not result in visuomotor activation in lateral cerebellum (lobule VI/Crus I), whereas frequent (25 Hz) intermittent visual feedback did. This is in contrast to the anterior intermediate cerebellum (lobule V/VI), which was consistently active across all force conditions compared with rest. Second, confirming previous observations, the parietal and premotor cortices were active during grip force with frequent visual feedback. The novel finding was that the parietal and premotor cortex were also active during grip force with infrequent visual feedback. Third, right inferior parietal lobule, dorsal premotor cortex, and ventral premotor cortex had greater activation in the frequent compared with the infrequent grip force condition. These findings demonstrate that the frequency of visual information reduces motor error and differentially modulates the neural activation related to visuomotor processing in the cerebellum, parietal cortex, and premotor cortex.

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Variable and intermittent grip force control in response to differing load force dynamics

Experimental Brain Research ◽

10.1007/s00221-018-5451-8 ◽

2018 ◽

Vol 237 (3) ◽

pp. 687-703 ◽

Cited By ~ 4

Author(s):

Francis M. Grover ◽

Patrick Nalepka ◽

Paula L. Silva ◽

Tamara Lorenz ◽

Michael A. Riley

Keyword(s):

Force Control ◽

Grip Force ◽

Load Force ◽

Force Dynamics ◽

Grip Force Control

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Wrist Action Affects Precision Grip Force

Journal of Neurophysiology ◽

10.1152/jn.1997.78.1.271 ◽

1997 ◽

Vol 78 (1) ◽

pp. 271-280 ◽

Cited By ~ 53

Author(s):

Mary M. Werremeyer ◽

Kelly J. Cole

Keyword(s):

Grip Force ◽

Precision Grip ◽

Load Force ◽

Myoelectric Activity ◽

Resistive Load ◽

Wrist Flexion ◽

Wrist Extension ◽

Hand Muscles ◽

Force Pulse ◽

Grasp Stability

Werremeyer, Mary M. and Kelly J. Cole. Wrist action affects precision grip force. J. Neurophysiol. 78: 271–280, 1997. When moving objects with a precision grip, fingertip forces normal to the object surface (grip force) change in parallel with forces tangential to the object (load force). We investigated whether voluntary wrist actions can affect grip force independent of load force, because the extrinsic finger muscles cross the wrist. Grip force increased with wrist angular speed during wrist motion in the horizontal plane, and was much larger than the increased tangential load at the fingertips or the reaction forces from linear acceleration of the test object. During wrist flexion the index finger muscles in the hand and forearm increased myoelectric activity; during wrist extension this myoelectric activity increased little, or decreased for some subjects. The grip force maxima coincided with wrist acceleration maxima, and grip force remained elevated when subjects held the wrist in extreme flexion or extension. Likewise, during isometric wrist actions the grip force increased even though the fingertip loads remained constant. A grip force “pulse” developed that increased with wrist force rate, followed by a static grip force while the wrist force was sustained. Subjects could not suppress the grip force pulse when provided visual feedback of their grip force. We conclude that the extrinsic hand muscles can be recruited to assist the intended wrist action, yielding higher grip-load ratios than those employed with the wrist at rest. This added drive to hand muscles overcame any loss in muscle force while the extrinsic finger flexors shortened during wrist flexion motion. During wrist extension motion grip force increases apparently occurred from eccentric contraction of the extrinsic finger flexors. The coactivation of hand closing muscles with other wrist muscles also may result in part from a general motor facilitation, because grip force increased during isometric knee extension. However, these increases were related weakly to the knee force. The observed muscle coactivation, from all sources, may contribute to grasp stability. For example, when transporting grasped objects, upper limb accelerations simultaneously produce inertial torques at the wrist that must be resisted, and inertial loads at the fingertips from the object that must be offset by increased grip force. The muscle coactivation described here would cause similarly timed pulses in the wrist force and grip force. However, grip-load coupling from this mechanism would not contribute much to grasp stability when small wrist forces are required, such as for slow movements or when the object's total resistive load is small.

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Flexible organization of grip force control during movement frequency scaling

Journal of Neurophysiology ◽

10.1152/jn.00416.2019 ◽

2019 ◽

Vol 122 (6) ◽

pp. 2304-2315

Author(s):

Francis M. Grover ◽

Sarah M. Schwab ◽

Paula L. Silva ◽

Tamara Lorenz ◽

Michael A. Riley

Keyword(s):

Force Control ◽

Grip Force ◽

Sagittal Plane ◽

Oscillation Amplitude ◽

Load Force ◽

Force Load ◽

Grip Force Control ◽

Force Coupling ◽

Tightly Coupled ◽

Oscillation Frequencies

The grip force applied to maintain grasp of a handheld object has been typically reported as tightly coupled to the load force exerted by the object as it is actively manipulated, occurring proportionally and consistently in phase with changes in load force. However, continuous grip force-load force coupling breaks down when overall load force levels and oscillation amplitudes are lower (Grover F, Lamb M, Bonnette S, Silva PL, Lorenz T, Riley MA. Exp Brain Res 236: 2531–2544, 2018) or more predictable (Grover FM, Nalepka P, Silva PL, Lorenz T, Riley MA. Exp Brain Res 237: 687–703, 2019). Under these circumstances, grip force is instead only intermittently coupled to load force; continuous coupling is prompted only when load force levels or variations become sufficiently high or unpredictable. The current study investigated the nature of the transition between continuous and intermittent modes of grip force control by scaling the load force level and the oscillation amplitude continuously in time by means of scaling the required frequency of movement oscillations. Participants grasped a cylindrical object between the thumb and forefinger and oscillated their arm about the shoulder in the sagittal plane. Oscillation frequencies were paced with a metronome that scaled through an ascending or descending frequency progression. Due to greater accelerations, faster frequencies produced greater overall load force levels and more pronounced load oscillations. We observed smooth but nonlinear transitions between clear regimes of intermittent and continuous grip force-load force coordination, for both scaling directions, indicating that grip force control can flexibly reorganize as parameters affecting grasp (e.g., variations in load force) change over time. NEW & NOTEWORTHY Grip force (GF) is synchronously coupled to changing load forces (LF) during object manipulation when LF levels are high or unpredictable, but only intermittently coupled to LF during less challenging grasp conditions. This study characterized the nature of transitions between synchronous and intermittent GF-LF coupling, revealing a smooth but nonlinear change in intermittent GF modulation in response to continuous scaling of LF amplitude. Intermittent, “drift-and-act” control may provide an alternative framework for understanding GF-LF coupling.

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Importance of Cutaneous Feedback in Maintaining a Secure Grip During Manipulation of Hand-Held Objects

Journal of Neurophysiology ◽

10.1152/jn.00249.2002 ◽

2003 ◽

Vol 89 (2) ◽

pp. 665-671 ◽

Cited By ~ 181

Author(s):

Anne-Sophie Augurelle ◽

Allan M. Smith ◽

Thierry Lejeune ◽

Jean-Louis Thonnard

Keyword(s):

Internal Model ◽

Grip Force ◽

Tangential Force ◽

Safety Margin ◽

Background Level ◽

Load Force ◽

Initial Contact ◽

Phase Lag ◽

Cutaneous Sensation ◽

Hold Period

Previous research has shown that grip and load forces are modulated simultaneously during manipulation of a hand-held object. This close temporal coupling suggested that both forces are controlled by an internal model within the CNS that predicts the changes in tangential force on the fingers. The objective of the present study was to examine how the internal model would compensate for the loss of cutaneous sensation through local anesthesia of the index and thumb. Ten healthy adult subjects (5 men and 5 women aged 20–57 yr) were asked to grasp, lift, and hold stationary, a 250 g object for 20 s. Next, the subjects were asked to perform vertical oscillatory movements over a distance of 20 cm at a rate of 1.0 Hz for 30 s. Eleven trials were performed with intact sensation, and 11 trials after a local ring-block anesthesia of the index and thumb with bupivacain (5 mg/ml). During static holding, loss of cutaneous sensation produced a significant increase in the safety margin. However, the grip force declined significantly over the 20-s static hold period. During oscillatory arm movements, grip and load forces were continuously modulated together in a predictive manner as suggested by Flanagan and Wing. Again, the grip force declined over the 30-s movement, and 7/10 subjects dropped the object at least once. With intact sensation, the object was never dropped; but with the fingers anesthetized, it was dropped on 36% of the trials, and a significant slip occurred on a further 12%. The mean correlation between the grip and load forces for all subjects deteriorated from 0.71 with intact sensation to 0.48 after digital anesthesia. However, a cross-correlation calculated between the grip and load forces indicated that the phase lag was approximately zero both with and without digital anesthesia. Taken together, the data from the present study suggest that cutaneous afferents are required for setting and maintaining the background level of the grip force in addition to their phasic slip-detection function and their role in adapting the grip force/load force ratio to the friction on initial contact with an object. Finally, at a more theoretical level, they correct and maintain an internal model of the physical properties of hand-held objects.

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