Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunar syndrome

Abstract

We examined planning and execution of precision grasp in eight right-handed patients with a right pure motor or sensorimotor lacunar syndrome after a subcortical stroke and eight age-matched controls as they grasped and lifted an instrumented object whose weight could be varied without altering its visual appearance. Grip (normal) and load (tangential) forces at the fingertip-object interface were measured and the grip force rate (GFR) and load force rate (LFR) were derived. Planning of precision grasp was assessed by measurement of anticipatory scaling of peak GFR and peak LFR to object weight. Execution of precision grasp was assessed by measurement of both the timing and efficiency of grip-load force coordination: the pre-load phase duration (PLD) and the load phase duration (LPD) measured timing, whereas the grip force at load force onset (GFO) and the grip force at lift-off (GFL) measured efficiency. Subjects lifted a light and heavy object five times first with the RIGHT hand, then with the LEFT hand, and then once more with the RIGHT AFTER LEFT hand. Patients with stroke did not scale the peak LFR or peak GFR to object weight with the RIGHT hand even with repeated attempts; however, they scaled the peak LFR to object weight on the first lift with the RIGHT AFTER LEFT hand (P = 0.01). Patients also prolonged the PLD and LPD and produced excessive GFO and GFL for RIGHT hand lifts, but decreased the GFL for the heavy object (P = 0.016) with the RIGHT AFTER LEFT hand. Correlation of precision grasp variables from lifts with the RIGHT hand with clinical measures showed that anticipatory scaling of peak LFR and peak GFR did not correlate with clinical measures of hand function, whereas the PLD did (r = 0.88, P = 0.004). The results suggest that patients with right hemiparesis from a subcortical lesion of the corticospinal tract have a higher-order motor planning deficit. This planning deficit is dissociable from deficits in motor execution, is not captured by routine clinical assessment, and is correctable by transfer of information from the unaffected hemisphere. A rehabilitation strategy that involves practice with the left hand prior to practice with the right hand may improve planning of grasping behaviour in patients with right hemiparesis.

Fingertip Force Planning During Grasp Is Disrupted by Impaired Sensorimotor Integration in Children With Hemiplegic Cerebral Palsy

“…Similar to the healthy children and adults, children with CP were able to transfer the anticipatory control between the two hands; following several lifts with the noninvolved hand, anticipatory control, reflected by force rates that appropriately reflect the object's weight, is immediately present in the involved hand (10). A similar transfer from the non-involved to the involved hand has been observed in adults with hemiplegia (11). Based on this finding, it was hypothesized that the impaired anticipatory control in the involved hand is the result of impaired or indistinct sensory mechanisms signaling the object's physical characteristics (10,12).…”

Quantifying feedforward control: a linear scaling model for fingertip forces and object weight

“…However, a clear difference in PLFR values between light and heavy objects was not seen in a population of patients with stroke despite several practice trials suggesting a lack of feedforward control poststroke (Raghavan et al 2006). However, the degree of impairment of feedforward control and the reason for the impairment have been difficult to quantify.…”

“…Force and EMG data were imported to and processed with MATLAB (The MathWorks, Natick, MA). Both grip and load forces were measured, but for the purpose of this study the computations pertain to load forces only, because it has been shown that when the friction at the grip surface is constant, feedforward control to object weight depends on the load forces (Raghavan et al 2006). Object liftoff was determined from the plate signals.…”

“…Studies from several laboratories, including ours, have shown that feedforward control of grasping forces is impaired after injury to the central nervous system, for example, after stroke despite reasonable practice with the affected hand Nowak et al 2003;Raghavan et al 2006Raghavan et al , 2010, suggesting that patients may be unable to effectively sense the error with their affected hand and/or integrate it with motor output, and that their motor systems are therefore unable to learn to execute tasks optimally. Skilled hand function requires that we constantly adapt our motor responses according to the properties of the objects we encounter, such as their weight, texture, or shape.…”

Losing control

“…Although neurorehabilitation is based on the assumption that patients can still learn, 5 relatively few studies have examined the effect of brain or spinal injury on motor learning itself. [6][7][8] It is a formidable challenge to compare learning capacity between groups with different initial levels of performance. If learning curves are compared, as was done in this study, the result can go in opposite directions depending on whether additive or multiplicative measures are used to assess learning.…”