Functional effect of short-term immobilization: Kinematic changes and recovery on reaching-to-grasp
Highlights
► Ten hours of right hand immobilization affected the kinematic of reaching-to-grasp. ► After immobilization we found an extended reach duration and deceleration phase. ► A full recovery was observed in the trial-by-trial repetitions of the task. ► This improvement was well fitted by an exponential function.
Introduction
Plasticity is an intrinsic property of the human brain that exhibits itself during the whole lifespan (Sanes and Donoghue, 2000, Jones and Lederman, 2006). It has been documented by using two main approaches: the first refers to brain changes related to an increase of sensory inputs and motor outputs (see for a review Pascual-Leone et al., 2005), while the second concerns the deprivation of these signals (e.g. Kaas, 2000). In this theoretical framework an important contribution is given by the recent model of short-term limb immobilization in healthy participants. Authors typically asked young subjects not to use their upper-limb for a limited period of time in order to verify the central effect induced by the non-use. For instance, Facchini et al. (2002) through Transcranial Magnetic Stimulation (TMS) recorded the amplitude of motor-evoked responses (MEP) after 4 days of ring and little fingers’ immobilization. They found an important decrease of motor cortex excitability contralateral to the immobilized limb. A similar effect was subsequently confirmed by Huber et al. (2006) following 12 h of upper-limb non-use and by our group in a recent study aimed to verify the role of the left free arm’s use during right hand immobilization (Avanzino et al., 2011). Beside a general agreement about the cortical changes induced by immobilization in healthy participants, little is known on the functional effects on motor behavior (Moisello et al., 2008).
As far as we know, alterations in the kinematic of a motor task after short-term immobilization were reported only in planar out-and-back movements executed with a digitizing tablet (Huber et al., 2006, Moisello et al., 2008). Here, we would like to extend these previous findings investigating the effect of 10 h of right hand immobilization in a different motor task: the reaching-to-grasp. It represents a daily life common motor behavior, fundamental for interaction with the surrounding environment. Moreover, reaching-to-grasp requires several visuo-motor transformations (see for a review Castiello, 2005). In fact, in order to plan the trajectory to bring the hand to the object and grasp it properly, visual and proprioceptive sources are essential to compute the current hand configuration and the arm posture. Previous studies suggest that this information is continuously updated through motion (for a review Wolpert and Ghahramani, 2000). Because movements are completely prevented during immobilization, one could suppose that the planning of reaching-to-grasp task is not supported by these inputs after non-use, leading to kinematic changes. Conversely, no effect after immobilization could be observed at least for two main reasons. First, our sensorimotor system seems to be robust to a brief period of immobilization, as during everyday life after comparable common experience of hypo-activity (like after long travels in airplane). Second, because the reaching-to-grasp is a very common activity, subjects might be so widely trained in the task that behavioral alterations would not be measurable. Moreover, it is worth to note that the reaching-to-grasp task involves a continuum of feedforward and feedback processes (Seidler et al., 2004). Predictions about the state of the motor system and environment in addition to sensory feedback can be used to update parameters of the next motion (e.g. Gentilucci et al., 1997). Thus, repeating the task trial-by-trial (i.e. 15 times) could give the subjects some important inputs to “recalibrate” the system after immobilization. To verify this hypothesis, possible changes in motor performance during trial repetitions were investigated.
Section snippets
Participants
Seven healthy volunteers (four female) participated in the study (mean age 27 ± 1.07 years, range 25–29). All participants were right handed, as determined by the Edinburgh Handedness Inventory (Oldfield, 1971). They reported normal or corrected-to-normal vision, no previous history of neurological disorders or recent orthopedic problems for the right upper limb. All subjects gave their written consent to participate in the study, which was performed with approval of the local ethics committee and
Results
Statistical analysis revealed that the reach duration values were equal in all the observations collected in the baseline conditions (see Fig. 3, upper panel). This finding excludes any general learning effect due to the repetitions of the task in different days.
However, in the first trial after immobilization, participants spent more time (974.3 ms, DAY × TRIAL: F(3, 18) = 5.4, p = .008) than in baseline 1, 2 and 3 (mean value: 679.6 ms). Importantly, after immobilization the first trial was
Discussion
As far as we know, this is the first demonstration of modifications in the kinematics of a reaching-to-grasp induced by a short-term period of immobilization in healthy subjects. Specifically, as soon as the bandage was removed subjects were still able to perform the reaching-to-grasp task but with a modified kinematic of the transport phase. On the contrary, no significant effect was observed for the grasping component that remained unvaried after immobilization. Precisely, the largest
Acknowledgements
We thank Gabriel Baud-Bovy for the helpful comments on the manuscript and Laura Taverna (3d Graphic designer at Robotics, Brain and Cognitive Sciences, Istituto Italiano di Tecnologia) for graphic elaboration of Fig. 1.
References (36)
- et al.
The relationship between human long-latency somatosensory evoked potentials recorded from the cortical surface and from the scalp
Electroencephalogr Clin Neurophysiol
(1992) - et al.
Gait-dependent motor memory facilitation in covert movement execution
Brain Res Cogn Brain Res
(2004) - et al.
Time-related changes of excitability of the human motor system contingent upon immobilisation of the ring and little fingers
Clin Neurophysiol
(2002) The reorganization of somatosensory and motor cortex after peripheral nerve or spinal cord injury in primates
Prog Brain Res
(2000)Internal models for motor control and trajectory planning
Curr Opin Neurobiol
(1999)- et al.
Human sensorimotor learning: adaptation, skill, and beyond
Curr Opin Neurobiol
(2011) - et al.
Immobilization impairs tactile perception and shrinks somatosensory cortical maps
Curr Biol
(2009) The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
(1971)- et al.
Does order and timing in performance of imagined and actual movements affect the motor imagery process? The duration of walking and writing task
Behav Brain Res
(2002) - et al.
Feedforward and feedback processes in motor control
Neuroimage
(2004)
Modulation of motor cortex excitability after upper limb immobilization
Clin Neurophysiol
Use-dependent hemispheric balance
J Neurosci
The neuroscience of grasping
Nat Rev Neurosci
The information capacity of the human motor system in controlling the amplitude of movement
J Exp Psychol
Short-term immobilization has a minimal effect on the strength and fatigability of a human hand muscle
J Appl Physiol
The role of proprioception in the control of prehension movements: a kinematic study in a peripherally deafferented patient and in normal subjects
Exp Brain Res
Tactile input of the hand and the control of reaching to grasp movements
Exp Brain Res
Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity
Nat Neurosci
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