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Intermanual transfer of sensorimotor memory for grip force when lifting objects: The role of wrist angulation
Clinical Neurophysiology 121 (2010) 402–407
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Intermanual transfer of sensorimotor memory for grip force when lifting objects: The role of wrist angulation Djamel Bensmail a,b,c, Anna-Sophia Sarfeld a, Gereon R. Fink a,e, Dennis A. Nowak a,d,* a
Department of Neurology, University Hospital, University of Cologne, Cologne, Germany Department of Physical Medicine and Rehabilitation, Hôpital R. Poincaré, Garches, AP-HP, University of Versailles Saint-Quentin, France c Laboratoire de Neurophysique et Physiologie, University Paris Descartes, CNRS UMR 8119, France d Hospital for Neurosurgery and Neurology, Kipfenberg, Germany e Institute of Neuroscience and Medicine (INM-3), Cognitive Neurology, Research Centre Jülich, Jülich, Germany b
a r t i c l e
i n f o
Article history: Accepted 8 November 2009 Available online 9 December 2009 Keywords: Grip force Memory Prediction Grasping Intermanual transfer
a b s t r a c t Objective: To investigate the mechanisms underlying the intermanual transfer of sensorimotor memory when lifting an object. Methods: Twenty healthy subjects grasped and lifted an object with constant mechanical properties with the right hand (RH) first and then with the left hand (LH). Ten of the subjects lifted the object with the RH in a regular wrist angulation (WA), followed by lifts with the LH in a regular WA. The remaining 10 subjects lifted the object with the RH in a hyper-flexed WA, followed by lifts with the LH in a regular WA. Results: Subjects generated greater peak grip force (GF) rates, grip and lift forces when lifting the object with the wrist in a regular WA compared to lifts with the wrist in hyper-flexion. Importantly, subjects transferred the predictive scaling of GF from the RH to the LH, regardless of the WA. Conclusions: Biomechanical properties of the object do not seem to be used by the CNS as a first line information to evaluate GF when handling an object or transferring information about the grasp to the opposite hemisphere. Significance: The predictive scaling of GF rather reflects an internal sense of effort than an internal representation of the mechanical object properties. Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction When grasping and lifting an object, people scale their grip forces in anticipation of the expected weight of the object (Johansson and Westling, 1988). In particular, we must exert sufficient grip force (normal to the object’s surface) to stabilize the object against the lift force (tangential to the surface) caused by the effects of gravity. Physical object properties, such as weight, surface frictions and shape, impose constraints on the applied grip forces, regarding their magnitude and points of application, necessary to prevent the object from slipping (Johansson and Westling, 1984; Jenmalm and Johansson, 1997). It has been shown that the balance between the grip force and the lift force is programmed to match the physical object properties, such as the friction at the skin–object interface and the object weight (for a recent review see Flanagan et al. (2009)). When lifting an object for the first time, grip force is programmed based on
* Corresponding author. Address: Klinik Kipfenberg, Neurochirurgische und Neurologische Fachklinik, Kindinger Strasse 13, D-85110 Kipfenberg, Germany. Tel.: +49 (0)8465 175 100; fax: +49 (0)8465 175 184. E-mail address: [email protected] (D.A. Nowak).
visual size cues (Gordon et al., 1991a,b, 1993). Within a few lifts of the same object, accurate predictive scaling of grip force is observed (Johansson and Westling, 1988). In this context the peak rate of grip force increase is considered a measure of prediction as it occurs prior to or at the time of object lift-off, well before somatosensory information about weight becomes available (Johansson and Westling, 1988). Predictive grip force scaling is maintained in long-term memory as reflected by our ability to generate accurate forces up to 24 h after first lifting an object (Flanagan et al., 2001). It has been suggested that this rapid learning and maintenance of predictive grip force scaling is related to an internal representation of the physical object properties (Johansson and Westling, 1988; Flanagan and Wing, 1997; Flanagan et al., 2006). In everyday manual activities, we often grasp and lift objects with both hands in alternation or transfer an object from one hand to the other. The question is how the central nervous system transfers sensorimotor information obtained from previous lifts of particular objects between hands. Gordon and colleagues (1994) have shown accurate intermanual transfer of weight information when lifting objects with constant mechanical properties in a precision grip even without visual feedback cues. In contrast, no or limited
1388-2457/$36.00 Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2009.11.010
D. Bensmail et al. / Clinical Neurophysiology 121 (2010) 402–407
transfer of sensorimotor performance between hands was found when complex loads were applied to the hand during goal-directed reaching (Malfait and Ostry, 2004; Criscimagna-Hemminger et al., 2003). Recently, Chang and co-workers (2008) showed that people use sensorimotor and not perceptual representations when transferring information about object weight from one hand to the other. Moreover, an accurate sensorimotor memory for grip forces can be formed by either squeezing an object with a certain force or lifting an object with a similar force (Quaney et al., 2003). The latter finding suggests that the sensorimotor memory rather reflects a sense of effort of the most recent action than an internal representation of the mechanical object properties. In a recent study (Bensmail et al., 2009), we have shown that wrist angulation has an impact on grip force scaling when lifting an object with constant mechanical properties. Subjects generated greater grip forces when lifting an object with the wrist hyper-extended and smaller grip forces when lifting an object with the wrist hyper-flexed, compared to a regular wrist angulation of 15° extension. The observation that people easily transfer the relevant forces in between hands (Gordon et al., 1994) and use different force levels when lifting an object depending on wrist angulation (Bensmail et al., 2009) could provide useful clues to improve our understanding of the details underlying the internal formation of sensorimotor memories. The present study was designed to further investigate this issue: Healthy right-handed subjects lifted an object with constant physical properties ten times first with the right hand followed by a series of ten lifts with the left hand. For lifts with the right hand wrist angulation was either in 15° extension (regular angulation) or hyper-flexed. For lifts with the left hand wrist angulation was always regular. In case the central nervous system uses the mechanical object properties to guide future motor commands of the left hand after lifting with the right hand, we expect that
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subjects scale predictive grip forces according to the object properties and not in dependence of wrist angulation. In case, however, the central nervous system uses a sense of effort related to the most recent motor action of the right hand to select appropriate forces for the left hand, we expect that subjects apply similar forces at either hand depending on the wrist angulation used during right hand lifts. 2. Material and methods 2.1. Participants Twenty healthy subjects (11 females, 9 males; mean age: 28 ± 4 years; age range: 24–39 years) participated. All subjects were right-handed according to a handedness questionnaire (Crovitz and Zener, 1965). None of the subjects had orthopedic or neurological disease of the upper limbs. Vision was normal or corrected to normal. Informed consent was obtained from each subject prior to testing and the procedures had been approved by the local Ethics Committee. 2.2. Instrumented object Participants grasped and lifted a cylindrical and cordless instrumented object (Nowak, 2008). Subjects first grasped ten times with their right, i.e. dominant hand, followed by ten lifts with their left hand. The object and the configuration of the fingers used to grasp it are illustrated in Fig. 1a. The object had a diameter of 9.0 cm and a width of 4.0 cm. The mass of the object was 300 g. Grip surfaces were covered with sandpaper of a medium grain (No. 240) in all trials performed. The object incorporated a force sensor for grip force registration (0–80 N, accuracy of ± 0.1 N) and linear accelera-
Fig. 1. (a) Illustration of the configuration of the hand used to grasp and lift the instrumented object and the forces generated by a grip-lift trial. (b) The orientation of the object was varied along its Z-axis during the experiment between three different positions: a neutral position with the grip surfaces aligned with the parasagittal plane of reaching (preferred, regular wrist angulation, WR) and orientation of the grip surfaces at 90° angulation in relation to the parasagittal plane (parafrontal plane) (maximum wrist flexion, WF). The object was not moved from the target position, but rotated along its Z-axis during the experiment.
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tion sensors (range: ±50 m/s2, accuracy: ±0.2 m/s2) for registration of acceleration signals in three dimensions. The center of mass of the object was halfway vertically below the points at which the fingers contacted its surfaces to minimize tilts or torques during the lifts. Recorded grip force and acceleration data were A-to-D converted with a sampling rate of 100 Hz and stored within the object. Data were transferred to a personal computer for off-line analysis following each experimental setting with a single subject. 2.3. Procedures The experiments were carried out in a quiet room with constant illumination. Prior to each experiment, one single experimenter (DB) explained the experiments to the subjects and demonstrated correct task performance. The different movements were practiced 2–3 times prior to the experimental session. The experimenter observed the subjects during the experiments. All subjects performed the experiments according to the instructions. Participants were seated on a stable chair in front of a table. The object was placed at a target position on the table in a parasagittal plane across the acromion of each arm so that reaching for it required only minimal shoulder movements. The distance of the object was at 100% of the length from the subject’s acromion to the carpo-metacarpal joint of the right and left arms. The orientation of the object was varied along its Z-axis during the experiment (see Fig. 1b): a neutral position with the grip surfaces aligned with the parasagittal plane (preferred, regular wrist angulation, 15° extension, RW) and orientation of the grip surfaces at 90° angulation in relation to the parasagittal plane (maximum wrist flexion, WF). The object was not moved from the target position, but rotated along its Z-axis during the experiment (see Fig. 1b). Subjects placed the hand on a starting point marked on the table with the hand closed and the forearm in an intermediate position between pronation and supination and started to reach for the object after a go signal provided verbally by the experimenter. Subjects grasped the object between the thumb and other fingers in opposition, lifted it 5 cm above the table (indicated by a marker), held it stationary for 2 s, and then replaced it. There was an interval of 5 s between each grip-lift trial. Subjects were asked to carry out movements at a comfortable speed. The experimenter assured a qualitative similarity of the subjects’ task performance by visual monitoring and, if necessary, oral feedback. Ten subjects performed ten grip-lift trials with the right hand with the wrist in a regular angulation, followed by ten lifts with the left hand with the wrist in a regular angulation. Ten different subjects performed ten lifts with the right hand with maximum wrist flexion, followed by ten lifts with the left hand with the wrist in regular angulation. At the beginning and end of the experiment participants were asked to grasp and lift the object in each wrist angulation with either hand and slowly separate the thumb and opposing fingers until it dropped. The grip forces obtained at the time the object started to slip (slip forces) are representative of the minimum grip force necessary to prevent the object slipping (Johansson and Westling, 1984, 1988). This procedure was carried out twice for each wrist angulation and hand. There were no significant differences between slip forces for each wrist angulation and hand at the beginning and end of the experiments. This indicates that differences in grip force for lifts in each wrist angulation did not reflect changes in friction at the skin-object interface (Johansson and Westling, 1984, 1988). 2.4. Data analysis and statistics The following parameters were analyzed for each grip-lift trial performed during the experiment: (1) peak lift force, (2) peak rate
of grip force increase, (3) peak grip force and (4) the ratio between peak grip and lift forces. Peak lift force was calculated from the product of the object mass and the vectorial summation of accelerations in three dimensions including gravity. The ratio between peak grip force and peak lift force was calculated to assess the efficiency of grip force scaling in relation to lift force. Student t-tests were conducted to compare the kinetic parameters from the two groups of subjects (RW and WF) during trials performed with the right hand. Repeated measure ANOVAs were performed to assess the effect of ‘‘sequence” (RW–RW, WF–RW) and ‘‘hand” (right or left hand) on each parameter. We compared the average of the last two lifts performed with the right hand and the average of the first two lifts performed with the left hand (Johansson and Westling, 1984, 1988; Nowak et al., 2004). Tukey honest significant differences-Test was used for pair-wise post hoc comparisons. A P-value of 0.05 was considered statistically significant. 3. Results 3.1. Effect of wrist angulation on force scaling Recently, we have shown that healthy subjects generate smaller grip forces when lifting an object with the wrist in maximum flexion and greater grip forces when lifting an object in maximum wrist extension, compared to lifts of an object with the wrist in a regular angulation at 15° extension (Bensmail et al., 2009). In the present experiments, peak grip forces were greater for lifts in regular wrist angulation compared to lifts with the wrist in maximum flexion (t = 2.82, df = 14.22, P = 0.01). The difference between regular and hyper-flexed wrist angulations on grip force scaling was also significant for the force ratios (t = 2.84, df = 15.19, P = 0.01). The difference was not significant for the peak rate of grip force increase and the lift force (t = 1.68, df = 9.75, P = 0.12; t = 0.87, df = 11.75, P = 0.40, respectively). 3.2. Intermanual transfer of force scaling Peak grip forces differed dependent upon wrist angulation. A significant effect of the factor ‘‘sequence” was found (F(1,72) = 13.1; P = 0.0005) which indicates that subjects generated smaller peak grip forces for lifts in the sequence WF–RW (mean ± SE = 10.85 ± 0.46) in comparison to the sequence RW–RW (mean ± SE = 17.39 ± 0.30) (see Fig. 2b). In contrast, we did not observed an effect of ‘‘hand” on peak grip forces. The interaction between ‘‘sequence” and ‘‘hand” factors was not significant. As for the peak grip force rate, we found a significant effect of the factor ‘‘sequence” on peak rates of grip force increase (F(1,72) = 8.91; P = 0.004) (mean = 50.92 ± 1.49 with WF–RW sequence versus mean = 87.04 ± 5.14 with RW–RW sequence). In contrast, no effect of ‘‘hand” was observed (see Fig. 2a). Table 1 describe for each kinetic parameter the percentage of difference between the different conditions. It clearly shows the effect of the factor ‘‘sequence” and the absence of effect of the factor ‘‘hand”. A significant effect of the factor ‘‘sequence” was also found for peak lift forces (F(1,72) = 4.56; P = 0.03), suggesting that the scaling of peak lift forces depends on the angulation of the wrist used in the first set of lifts performed rather than on the mechanical object properties (see Fig. 2c). No significant effects of ‘‘hand” on peak lift forces were found. As for the other kinetic parameters, we found a significant effect of ‘‘sequence” on the force ratio (F(1,72) = 10.9; P = 0.001), whereas ‘‘hand” developed no significant effect. That is, force ratios were smaller for lifts with maximum wrist flexion (mean ± SE = 3.13 ± 0.10), compared to lifts with regular wrist angulation (mean ± SE = 4.66 ± 0.10). This effect was transferred to the left hand. That is, force ratios for lifts with the left hand
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Fig. 2. Illustration of peak rates of grip force increase 2(a), peak grip forces 2(b), peak lift forces 2(c) and ratios between peak grip and lift forces 2(d) obtained for the first and last grip-lift trials performed in sets of 10 trials with each sequence and each hand. Average values and standard errors of the mean are shown. FW–RW: 10 lifts performed with the right hand with the wrist in maximum flexion, followed by 10 lifts with the left hand with the wrist in regular angulation. RW–RW: l0 lifts performed with the right hand with the wrist in regular angulation followed by 10 lifts performed with the left hand with the wrist in regular angulation. First: 2 first trials, Last: 2 last trials, R: right hand, L: left hand.
(in regular wrist angulation) were smaller when preceded by lifts of the right hand in maximum wrist angulation, but greater when preceded by lifts of the right hand in regular wrist angulation (P = 0.02) (see Fig. 2d). The interaction between ‘‘sequence” and ‘‘hand” factors was not significant for all the studied parameters. 4. Discussion We investigated whether the transfer of force scaling between hands depends on an internal representation of the mechanical object properties or rather on an internal sense of effort related to the most recent action. Healthy right-handed subjects lifted an object with constant physical properties ten times first with the right hand followed by a series of ten lifts with the left hand. For lifts
Table 1 Percentage of difference between the different conditions for each kinetic parameter.
Peak GFR Peak GF Peak LF Force ratio
Right hand WR–WF (%)
Left hand WR–WF (%)
WF–WR right–left (%)
WR–WR right-left (%)
40 22.04 6 16.40
41.50 37.61 6 32.83
4.20 1.36 1.42 0.6
1.74 18.86 1.34 20.17
GFR: grip force rate, GF: grip force, LF: lift force. Right hand WR–WF = % of difference between lifts performed with the right hand with the wrist in a regular or a flexed position for each kinetic parameter. Left hand WR–WF = % of difference for each kinetic parameter between lifts performed with the left hand with the wrist in a regular angulation when lifts were preceded by lifts with the right hand with the wrist in a regular or a flexed position. WF–WR right– left = % of difference for each kinetic parameter between right and left hand in the WF–WR sequence group of subjects. WR–WR right–left = % of difference for each kinetic parameter between right and left hand in the WR–WR sequence group of subjects.
with the right hand, wrist angulation was either in 15° extension (regular angulation) or at maximum flexion. For lifts with the left hand, wrist angulation was always regular. We confirmed the results of a previous study that wrist angulation impacts on the scaling of grip forces (Bensmail et al., 2009). That is subjects generated smaller grip forces when lifting the object with the wrist in maximum flexion compared to lifts with the wrist in regular angulation. In addition, force levels generated with the right hand depended upon wrist angulation (either regular or maximum flexion), and were transferred to the opposite left hand, which lifted the object in regular wrist angulation. These data imply that the sensorimotor memory for grip forces rather depends on an internal sense of effort than being a reflection of the mechanical object properties. Wrist extension and hyper-flexion modify proprioceptive input from muscles of the hand and forearm towards central force control instances. Extension of the wrist causes stretching of the extrinsic finger flexors, whereas hyper-flexion causes shortening of the extrinsic finger flexors. The modification of afferent, proprioceptive input associated with a change in wrist angulation may shape the excitability maps of motor output at a cortical or spinal level (Devanne et al., 2002; Ginanneschi et al., 2005, 2006; Gagné and Schneider, 2007). It has been demonstrated that voluntary movements of the wrist when holding an object influence the scaling of grip force independent of the produced loads (Werremeyer and Cole, 1997). Grip force increased with wrist angular speed during wrist motion in the horizontal plane, and this increase was essentially greater than the amount of inertial loads added on the hand-held object resulting from the movement. Interestingly, this overshoot in grip force was greater during wrist flexion, compared to wrist extension, and accompanied by increased electric muscle activity of the superficial finger flexors and first dorsal interosseus muscle (Werremeyer and Cole, 1997). This finding fits well with the observation of an increase in cortico-spinal activity
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towards the intrinsic hand muscles when grasping an object between index finger and thumb in wrist flexion (Gagné and Schneider, 2007), but differs from our observation that grip force was higher when lifting the object with the wrist in moderate extension than in hyper-flexion. It might be that the excitability of extrinsic and intrinsic hand muscles varies in an opposite way during these movements. Further studies are needed to test this hypothesis. When grasping and lifting an object, we rapidly learn to scale our grip forces precisely to the mechanical object properties, such as weight and surface friction (Johansson and Westling, 1988). In addition, we retain the ability to scale grip force according to the individual object requirements in long-term memory for up to 24 h (Gordon et al., 1993, 1994). In the context of the memory processes underlying the precise scaling of grip forces, two hypotheses have been proposed. Some authors argue in favor of the idea that people store information about the mechanical object properties within their brain and use this information to guide future motor commands (Flanagan et al., 2006). In contrast, other authors have argued in favor of the idea that subjects use memories related to their own actions (a sense of effort of forces or motor commands) rather than a memory related to the object properties (Quaney et al., 2003). Quaney and colleagues (2003) have shown that the grip force applied to lift an object with known properties can be increased by similar amounts when either performing a lift of a heavier object or simply pinching a force transducer with a target force reflecting the weight to be counteracted by lifting the heavier object. These data suggest that people remember the forces they have generated and that the sensorimotor memory is not specific for lifting an object. Interestingly, a period of muscle vibration applied to selective hand muscles normally involved in the motor act of grasping and lifting an object also influenced the grip force subsequently used to lift a known object either with the same or opposite hand (Nowak et al., 2004). Taken together these findings provide strong evidence that the memory processes underlying the predictive selection of grip forces when grasping and lifting a known object are neither uniquely related to the mechanical object properties nor to the act of grasping, but also may reflect the most recent sensory feedback from the muscles involved in grasping. Our data extend these previous findings by showing that grip forces generated by the right hand depended on the wrist angulation applied during the lift and that exactly these forces were transferred to the left hand, which lifted the same object in a regular wrist angulation. In other words, our data argue in favor of an internal representation of self-generated forces when scaling grip forces during object lifts. In a previous study, Quaney and colleagues (2003) showed that peak lift force produced when a 4 N lift force was preceded by a 8 N lift was significantly higher than the peak lift force produced when a 4 N lift force was preceded by a 4 N lift or 8 N pinch. In contrast, the peak grip force was significantly higher when a 8 N lift or a 8 N pinch preceded the 4 N lift, compared to the peak grip force generated when a 4 N lift was preceded by a 4 N lift. These authors concluded that we use an object-based memory when lifting an object, but an action-based memory when pinching, given that object properties such as load are unavailable. An explanation may be that different force scaling mechanisms are used for the grip and lift components of the grip-lift task. Our results show that the intermanual transfer of peak lift force depends on the peak lift force generated to lift the object with the opposite hand. Subjects produced smaller peak lift forces with the right hand when the wrist was in maximum flexion compared to regular wrist angulation. When lifting with the left hand they reproduced the lift forces generated with the right hand, suggesting that also the programming of peak lift force reflects internally stored memories related to action.
In a recent study, Cole (2008) showed that we routinely use rather information derived by visual analysis of an object’s size and shape, along with a memory of object density, than object weight to estimate the grip forces needed to handle common objects. However, it seems that action and perception are not strictly separated during visual analysis, dependent upon which component of an action is considered (Brenner and Smeets, 1996). In accordance with the data of Cole and co-workers (2008), we found that the memory of the most recent action overrules potential memories related to the mechanical object properties during intermanual transfer of grip and lift forces. Biomechanical properties of the object such as the weight do not seem to be used by the central nervous system as a first line information to evaluate grip force when handling an object or transferring information about the grasp to the opposite hemisphere. 4.1. Clinical implications Stroke or traumatic brain injury may cause an increased muscle tone, e.g. spasticity, or muscle contracture of the upper limb causing flexion deviation of the wrist within the horizontal plane (O’Dwyer et al., 1996; Pandyan et al., 2003). The overshoot in grip forces in relation to the lift forces to be observed at the affected hand after stroke has primarily been interpreted to reflect a strategy of the motor system to guarantee a stable grasp in the presence of sensorimotor dysfunction (McDonnell et al., 2006; Nowak et al., 2003). The changes in grip force scaling observed in stroke survivors might be influenced by deviation of the wrist in the horizontal plane, e.g. due to spasticity or contractures. Future studies should systematically address this issue. We found that the so-called sensorimotor memory used for intermanual transfer may be based on the motor commands used to handle an object rather than on the mechanical properties of the object. This observation may have an impact on rehabilitation techniques on stroke patients that make use of the unaffected hand to facilitate relearning of motor skills with the affected hand. The angulation of the wrist during training with the unaffected hand may influence the transfer of sensorimotor information to the affected hemisphere and potentially the motor skills to be produced with the affected hand. This should be taken into account when designing behavioral rehabilitation protocols focusing on hand motor control. Financial disclosures None of the authors has any financial disclosures regarding the present manuscript. Acknowledgements This work was supported by grants of the Deutsche Forschungsgemeinschaft (DFG, NO 737/5-1) and the Köln Fortune Programm (173/2006) to Dennis A. Nowak. Djamel Bensmail was supported by grants of Fondation Garches, SOFMER-IPSEN, Assistance Publique-Hôpitaux de Paris, Allergan and Medtronic. References Bensmail D, Sarfeld AS, Fink GR, Nowak DA. Sensorimotor processing in the grip-lift task: the impact of maximum wrist flexion/extension on force scaling. Clin Neurophysiol 2009;120:1588–95. Brenner E, Smeets JBJ. Size illusion influences how we lift but not how we grasp an object. Exp Brain Res 1996;111:473–6. Chang EC, Flanagan JR, Goodale MA. The intermanual transfer of anticipatory force control in precision grip lifting is not influenced by the perception of weight. Exp Brain Res 2008;185(2):319–29. Cole KJ. Lifting a familiar object: visual size analysis, not memory of object weight, scales lift force. Exp Brain Res 2008;188:551–7.
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Intermanual transfer of sensorimotor memory for grip force when lifting objects: The role of wrist angulation Djamel Bensmail a,b,c, Anna-Sophia Sarfeld a, Gereon R. Fink a,e, Dennis A. Nowak a,d,* a
Department of Neurology, University Hospital, University of Cologne, Cologne, Germany Department of Physical Medicine and Rehabilitation, Hôpital R. Poincaré, Garches, AP-HP, University of Versailles Saint-Quentin, France c Laboratoire de Neurophysique et Physiologie, University Paris Descartes, CNRS UMR 8119, France d Hospital for Neurosurgery and Neurology, Kipfenberg, Germany e Institute of Neuroscience and Medicine (INM-3), Cognitive Neurology, Research Centre Jülich, Jülich, Germany b
a r t i c l e
i n f o
Article history: Accepted 8 November 2009 Available online 9 December 2009 Keywords: Grip force Memory Prediction Grasping Intermanual transfer
a b s t r a c t Objective: To investigate the mechanisms underlying the intermanual transfer of sensorimotor memory when lifting an object. Methods: Twenty healthy subjects grasped and lifted an object with constant mechanical properties with the right hand (RH) first and then with the left hand (LH). Ten of the subjects lifted the object with the RH in a regular wrist angulation (WA), followed by lifts with the LH in a regular WA. The remaining 10 subjects lifted the object with the RH in a hyper-flexed WA, followed by lifts with the LH in a regular WA. Results: Subjects generated greater peak grip force (GF) rates, grip and lift forces when lifting the object with the wrist in a regular WA compared to lifts with the wrist in hyper-flexion. Importantly, subjects transferred the predictive scaling of GF from the RH to the LH, regardless of the WA. Conclusions: Biomechanical properties of the object do not seem to be used by the CNS as a first line information to evaluate GF when handling an object or transferring information about the grasp to the opposite hemisphere. Significance: The predictive scaling of GF rather reflects an internal sense of effort than an internal representation of the mechanical object properties. Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction When grasping and lifting an object, people scale their grip forces in anticipation of the expected weight of the object (Johansson and Westling, 1988). In particular, we must exert sufficient grip force (normal to the object’s surface) to stabilize the object against the lift force (tangential to the surface) caused by the effects of gravity. Physical object properties, such as weight, surface frictions and shape, impose constraints on the applied grip forces, regarding their magnitude and points of application, necessary to prevent the object from slipping (Johansson and Westling, 1984; Jenmalm and Johansson, 1997). It has been shown that the balance between the grip force and the lift force is programmed to match the physical object properties, such as the friction at the skin–object interface and the object weight (for a recent review see Flanagan et al. (2009)). When lifting an object for the first time, grip force is programmed based on
* Corresponding author. Address: Klinik Kipfenberg, Neurochirurgische und Neurologische Fachklinik, Kindinger Strasse 13, D-85110 Kipfenberg, Germany. Tel.: +49 (0)8465 175 100; fax: +49 (0)8465 175 184. E-mail address: [email protected] (D.A. Nowak).
visual size cues (Gordon et al., 1991a,b, 1993). Within a few lifts of the same object, accurate predictive scaling of grip force is observed (Johansson and Westling, 1988). In this context the peak rate of grip force increase is considered a measure of prediction as it occurs prior to or at the time of object lift-off, well before somatosensory information about weight becomes available (Johansson and Westling, 1988). Predictive grip force scaling is maintained in long-term memory as reflected by our ability to generate accurate forces up to 24 h after first lifting an object (Flanagan et al., 2001). It has been suggested that this rapid learning and maintenance of predictive grip force scaling is related to an internal representation of the physical object properties (Johansson and Westling, 1988; Flanagan and Wing, 1997; Flanagan et al., 2006). In everyday manual activities, we often grasp and lift objects with both hands in alternation or transfer an object from one hand to the other. The question is how the central nervous system transfers sensorimotor information obtained from previous lifts of particular objects between hands. Gordon and colleagues (1994) have shown accurate intermanual transfer of weight information when lifting objects with constant mechanical properties in a precision grip even without visual feedback cues. In contrast, no or limited
1388-2457/$36.00 Ó 2009 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2009.11.010
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transfer of sensorimotor performance between hands was found when complex loads were applied to the hand during goal-directed reaching (Malfait and Ostry, 2004; Criscimagna-Hemminger et al., 2003). Recently, Chang and co-workers (2008) showed that people use sensorimotor and not perceptual representations when transferring information about object weight from one hand to the other. Moreover, an accurate sensorimotor memory for grip forces can be formed by either squeezing an object with a certain force or lifting an object with a similar force (Quaney et al., 2003). The latter finding suggests that the sensorimotor memory rather reflects a sense of effort of the most recent action than an internal representation of the mechanical object properties. In a recent study (Bensmail et al., 2009), we have shown that wrist angulation has an impact on grip force scaling when lifting an object with constant mechanical properties. Subjects generated greater grip forces when lifting an object with the wrist hyper-extended and smaller grip forces when lifting an object with the wrist hyper-flexed, compared to a regular wrist angulation of 15° extension. The observation that people easily transfer the relevant forces in between hands (Gordon et al., 1994) and use different force levels when lifting an object depending on wrist angulation (Bensmail et al., 2009) could provide useful clues to improve our understanding of the details underlying the internal formation of sensorimotor memories. The present study was designed to further investigate this issue: Healthy right-handed subjects lifted an object with constant physical properties ten times first with the right hand followed by a series of ten lifts with the left hand. For lifts with the right hand wrist angulation was either in 15° extension (regular angulation) or hyper-flexed. For lifts with the left hand wrist angulation was always regular. In case the central nervous system uses the mechanical object properties to guide future motor commands of the left hand after lifting with the right hand, we expect that
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subjects scale predictive grip forces according to the object properties and not in dependence of wrist angulation. In case, however, the central nervous system uses a sense of effort related to the most recent motor action of the right hand to select appropriate forces for the left hand, we expect that subjects apply similar forces at either hand depending on the wrist angulation used during right hand lifts. 2. Material and methods 2.1. Participants Twenty healthy subjects (11 females, 9 males; mean age: 28 ± 4 years; age range: 24–39 years) participated. All subjects were right-handed according to a handedness questionnaire (Crovitz and Zener, 1965). None of the subjects had orthopedic or neurological disease of the upper limbs. Vision was normal or corrected to normal. Informed consent was obtained from each subject prior to testing and the procedures had been approved by the local Ethics Committee. 2.2. Instrumented object Participants grasped and lifted a cylindrical and cordless instrumented object (Nowak, 2008). Subjects first grasped ten times with their right, i.e. dominant hand, followed by ten lifts with their left hand. The object and the configuration of the fingers used to grasp it are illustrated in Fig. 1a. The object had a diameter of 9.0 cm and a width of 4.0 cm. The mass of the object was 300 g. Grip surfaces were covered with sandpaper of a medium grain (No. 240) in all trials performed. The object incorporated a force sensor for grip force registration (0–80 N, accuracy of ± 0.1 N) and linear accelera-
Fig. 1. (a) Illustration of the configuration of the hand used to grasp and lift the instrumented object and the forces generated by a grip-lift trial. (b) The orientation of the object was varied along its Z-axis during the experiment between three different positions: a neutral position with the grip surfaces aligned with the parasagittal plane of reaching (preferred, regular wrist angulation, WR) and orientation of the grip surfaces at 90° angulation in relation to the parasagittal plane (parafrontal plane) (maximum wrist flexion, WF). The object was not moved from the target position, but rotated along its Z-axis during the experiment.
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tion sensors (range: ±50 m/s2, accuracy: ±0.2 m/s2) for registration of acceleration signals in three dimensions. The center of mass of the object was halfway vertically below the points at which the fingers contacted its surfaces to minimize tilts or torques during the lifts. Recorded grip force and acceleration data were A-to-D converted with a sampling rate of 100 Hz and stored within the object. Data were transferred to a personal computer for off-line analysis following each experimental setting with a single subject. 2.3. Procedures The experiments were carried out in a quiet room with constant illumination. Prior to each experiment, one single experimenter (DB) explained the experiments to the subjects and demonstrated correct task performance. The different movements were practiced 2–3 times prior to the experimental session. The experimenter observed the subjects during the experiments. All subjects performed the experiments according to the instructions. Participants were seated on a stable chair in front of a table. The object was placed at a target position on the table in a parasagittal plane across the acromion of each arm so that reaching for it required only minimal shoulder movements. The distance of the object was at 100% of the length from the subject’s acromion to the carpo-metacarpal joint of the right and left arms. The orientation of the object was varied along its Z-axis during the experiment (see Fig. 1b): a neutral position with the grip surfaces aligned with the parasagittal plane (preferred, regular wrist angulation, 15° extension, RW) and orientation of the grip surfaces at 90° angulation in relation to the parasagittal plane (maximum wrist flexion, WF). The object was not moved from the target position, but rotated along its Z-axis during the experiment (see Fig. 1b). Subjects placed the hand on a starting point marked on the table with the hand closed and the forearm in an intermediate position between pronation and supination and started to reach for the object after a go signal provided verbally by the experimenter. Subjects grasped the object between the thumb and other fingers in opposition, lifted it 5 cm above the table (indicated by a marker), held it stationary for 2 s, and then replaced it. There was an interval of 5 s between each grip-lift trial. Subjects were asked to carry out movements at a comfortable speed. The experimenter assured a qualitative similarity of the subjects’ task performance by visual monitoring and, if necessary, oral feedback. Ten subjects performed ten grip-lift trials with the right hand with the wrist in a regular angulation, followed by ten lifts with the left hand with the wrist in a regular angulation. Ten different subjects performed ten lifts with the right hand with maximum wrist flexion, followed by ten lifts with the left hand with the wrist in regular angulation. At the beginning and end of the experiment participants were asked to grasp and lift the object in each wrist angulation with either hand and slowly separate the thumb and opposing fingers until it dropped. The grip forces obtained at the time the object started to slip (slip forces) are representative of the minimum grip force necessary to prevent the object slipping (Johansson and Westling, 1984, 1988). This procedure was carried out twice for each wrist angulation and hand. There were no significant differences between slip forces for each wrist angulation and hand at the beginning and end of the experiments. This indicates that differences in grip force for lifts in each wrist angulation did not reflect changes in friction at the skin-object interface (Johansson and Westling, 1984, 1988). 2.4. Data analysis and statistics The following parameters were analyzed for each grip-lift trial performed during the experiment: (1) peak lift force, (2) peak rate
of grip force increase, (3) peak grip force and (4) the ratio between peak grip and lift forces. Peak lift force was calculated from the product of the object mass and the vectorial summation of accelerations in three dimensions including gravity. The ratio between peak grip force and peak lift force was calculated to assess the efficiency of grip force scaling in relation to lift force. Student t-tests were conducted to compare the kinetic parameters from the two groups of subjects (RW and WF) during trials performed with the right hand. Repeated measure ANOVAs were performed to assess the effect of ‘‘sequence” (RW–RW, WF–RW) and ‘‘hand” (right or left hand) on each parameter. We compared the average of the last two lifts performed with the right hand and the average of the first two lifts performed with the left hand (Johansson and Westling, 1984, 1988; Nowak et al., 2004). Tukey honest significant differences-Test was used for pair-wise post hoc comparisons. A P-value of 0.05 was considered statistically significant. 3. Results 3.1. Effect of wrist angulation on force scaling Recently, we have shown that healthy subjects generate smaller grip forces when lifting an object with the wrist in maximum flexion and greater grip forces when lifting an object in maximum wrist extension, compared to lifts of an object with the wrist in a regular angulation at 15° extension (Bensmail et al., 2009). In the present experiments, peak grip forces were greater for lifts in regular wrist angulation compared to lifts with the wrist in maximum flexion (t = 2.82, df = 14.22, P = 0.01). The difference between regular and hyper-flexed wrist angulations on grip force scaling was also significant for the force ratios (t = 2.84, df = 15.19, P = 0.01). The difference was not significant for the peak rate of grip force increase and the lift force (t = 1.68, df = 9.75, P = 0.12; t = 0.87, df = 11.75, P = 0.40, respectively). 3.2. Intermanual transfer of force scaling Peak grip forces differed dependent upon wrist angulation. A significant effect of the factor ‘‘sequence” was found (F(1,72) = 13.1; P = 0.0005) which indicates that subjects generated smaller peak grip forces for lifts in the sequence WF–RW (mean ± SE = 10.85 ± 0.46) in comparison to the sequence RW–RW (mean ± SE = 17.39 ± 0.30) (see Fig. 2b). In contrast, we did not observed an effect of ‘‘hand” on peak grip forces. The interaction between ‘‘sequence” and ‘‘hand” factors was not significant. As for the peak grip force rate, we found a significant effect of the factor ‘‘sequence” on peak rates of grip force increase (F(1,72) = 8.91; P = 0.004) (mean = 50.92 ± 1.49 with WF–RW sequence versus mean = 87.04 ± 5.14 with RW–RW sequence). In contrast, no effect of ‘‘hand” was observed (see Fig. 2a). Table 1 describe for each kinetic parameter the percentage of difference between the different conditions. It clearly shows the effect of the factor ‘‘sequence” and the absence of effect of the factor ‘‘hand”. A significant effect of the factor ‘‘sequence” was also found for peak lift forces (F(1,72) = 4.56; P = 0.03), suggesting that the scaling of peak lift forces depends on the angulation of the wrist used in the first set of lifts performed rather than on the mechanical object properties (see Fig. 2c). No significant effects of ‘‘hand” on peak lift forces were found. As for the other kinetic parameters, we found a significant effect of ‘‘sequence” on the force ratio (F(1,72) = 10.9; P = 0.001), whereas ‘‘hand” developed no significant effect. That is, force ratios were smaller for lifts with maximum wrist flexion (mean ± SE = 3.13 ± 0.10), compared to lifts with regular wrist angulation (mean ± SE = 4.66 ± 0.10). This effect was transferred to the left hand. That is, force ratios for lifts with the left hand
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Fig. 2. Illustration of peak rates of grip force increase 2(a), peak grip forces 2(b), peak lift forces 2(c) and ratios between peak grip and lift forces 2(d) obtained for the first and last grip-lift trials performed in sets of 10 trials with each sequence and each hand. Average values and standard errors of the mean are shown. FW–RW: 10 lifts performed with the right hand with the wrist in maximum flexion, followed by 10 lifts with the left hand with the wrist in regular angulation. RW–RW: l0 lifts performed with the right hand with the wrist in regular angulation followed by 10 lifts performed with the left hand with the wrist in regular angulation. First: 2 first trials, Last: 2 last trials, R: right hand, L: left hand.
(in regular wrist angulation) were smaller when preceded by lifts of the right hand in maximum wrist angulation, but greater when preceded by lifts of the right hand in regular wrist angulation (P = 0.02) (see Fig. 2d). The interaction between ‘‘sequence” and ‘‘hand” factors was not significant for all the studied parameters. 4. Discussion We investigated whether the transfer of force scaling between hands depends on an internal representation of the mechanical object properties or rather on an internal sense of effort related to the most recent action. Healthy right-handed subjects lifted an object with constant physical properties ten times first with the right hand followed by a series of ten lifts with the left hand. For lifts
Table 1 Percentage of difference between the different conditions for each kinetic parameter.
Peak GFR Peak GF Peak LF Force ratio
Right hand WR–WF (%)
Left hand WR–WF (%)
WF–WR right–left (%)
WR–WR right-left (%)
40 22.04 6 16.40
41.50 37.61 6 32.83
4.20 1.36 1.42 0.6
1.74 18.86 1.34 20.17
GFR: grip force rate, GF: grip force, LF: lift force. Right hand WR–WF = % of difference between lifts performed with the right hand with the wrist in a regular or a flexed position for each kinetic parameter. Left hand WR–WF = % of difference for each kinetic parameter between lifts performed with the left hand with the wrist in a regular angulation when lifts were preceded by lifts with the right hand with the wrist in a regular or a flexed position. WF–WR right– left = % of difference for each kinetic parameter between right and left hand in the WF–WR sequence group of subjects. WR–WR right–left = % of difference for each kinetic parameter between right and left hand in the WR–WR sequence group of subjects.
with the right hand, wrist angulation was either in 15° extension (regular angulation) or at maximum flexion. For lifts with the left hand, wrist angulation was always regular. We confirmed the results of a previous study that wrist angulation impacts on the scaling of grip forces (Bensmail et al., 2009). That is subjects generated smaller grip forces when lifting the object with the wrist in maximum flexion compared to lifts with the wrist in regular angulation. In addition, force levels generated with the right hand depended upon wrist angulation (either regular or maximum flexion), and were transferred to the opposite left hand, which lifted the object in regular wrist angulation. These data imply that the sensorimotor memory for grip forces rather depends on an internal sense of effort than being a reflection of the mechanical object properties. Wrist extension and hyper-flexion modify proprioceptive input from muscles of the hand and forearm towards central force control instances. Extension of the wrist causes stretching of the extrinsic finger flexors, whereas hyper-flexion causes shortening of the extrinsic finger flexors. The modification of afferent, proprioceptive input associated with a change in wrist angulation may shape the excitability maps of motor output at a cortical or spinal level (Devanne et al., 2002; Ginanneschi et al., 2005, 2006; Gagné and Schneider, 2007). It has been demonstrated that voluntary movements of the wrist when holding an object influence the scaling of grip force independent of the produced loads (Werremeyer and Cole, 1997). Grip force increased with wrist angular speed during wrist motion in the horizontal plane, and this increase was essentially greater than the amount of inertial loads added on the hand-held object resulting from the movement. Interestingly, this overshoot in grip force was greater during wrist flexion, compared to wrist extension, and accompanied by increased electric muscle activity of the superficial finger flexors and first dorsal interosseus muscle (Werremeyer and Cole, 1997). This finding fits well with the observation of an increase in cortico-spinal activity
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towards the intrinsic hand muscles when grasping an object between index finger and thumb in wrist flexion (Gagné and Schneider, 2007), but differs from our observation that grip force was higher when lifting the object with the wrist in moderate extension than in hyper-flexion. It might be that the excitability of extrinsic and intrinsic hand muscles varies in an opposite way during these movements. Further studies are needed to test this hypothesis. When grasping and lifting an object, we rapidly learn to scale our grip forces precisely to the mechanical object properties, such as weight and surface friction (Johansson and Westling, 1988). In addition, we retain the ability to scale grip force according to the individual object requirements in long-term memory for up to 24 h (Gordon et al., 1993, 1994). In the context of the memory processes underlying the precise scaling of grip forces, two hypotheses have been proposed. Some authors argue in favor of the idea that people store information about the mechanical object properties within their brain and use this information to guide future motor commands (Flanagan et al., 2006). In contrast, other authors have argued in favor of the idea that subjects use memories related to their own actions (a sense of effort of forces or motor commands) rather than a memory related to the object properties (Quaney et al., 2003). Quaney and colleagues (2003) have shown that the grip force applied to lift an object with known properties can be increased by similar amounts when either performing a lift of a heavier object or simply pinching a force transducer with a target force reflecting the weight to be counteracted by lifting the heavier object. These data suggest that people remember the forces they have generated and that the sensorimotor memory is not specific for lifting an object. Interestingly, a period of muscle vibration applied to selective hand muscles normally involved in the motor act of grasping and lifting an object also influenced the grip force subsequently used to lift a known object either with the same or opposite hand (Nowak et al., 2004). Taken together these findings provide strong evidence that the memory processes underlying the predictive selection of grip forces when grasping and lifting a known object are neither uniquely related to the mechanical object properties nor to the act of grasping, but also may reflect the most recent sensory feedback from the muscles involved in grasping. Our data extend these previous findings by showing that grip forces generated by the right hand depended on the wrist angulation applied during the lift and that exactly these forces were transferred to the left hand, which lifted the same object in a regular wrist angulation. In other words, our data argue in favor of an internal representation of self-generated forces when scaling grip forces during object lifts. In a previous study, Quaney and colleagues (2003) showed that peak lift force produced when a 4 N lift force was preceded by a 8 N lift was significantly higher than the peak lift force produced when a 4 N lift force was preceded by a 4 N lift or 8 N pinch. In contrast, the peak grip force was significantly higher when a 8 N lift or a 8 N pinch preceded the 4 N lift, compared to the peak grip force generated when a 4 N lift was preceded by a 4 N lift. These authors concluded that we use an object-based memory when lifting an object, but an action-based memory when pinching, given that object properties such as load are unavailable. An explanation may be that different force scaling mechanisms are used for the grip and lift components of the grip-lift task. Our results show that the intermanual transfer of peak lift force depends on the peak lift force generated to lift the object with the opposite hand. Subjects produced smaller peak lift forces with the right hand when the wrist was in maximum flexion compared to regular wrist angulation. When lifting with the left hand they reproduced the lift forces generated with the right hand, suggesting that also the programming of peak lift force reflects internally stored memories related to action.
In a recent study, Cole (2008) showed that we routinely use rather information derived by visual analysis of an object’s size and shape, along with a memory of object density, than object weight to estimate the grip forces needed to handle common objects. However, it seems that action and perception are not strictly separated during visual analysis, dependent upon which component of an action is considered (Brenner and Smeets, 1996). In accordance with the data of Cole and co-workers (2008), we found that the memory of the most recent action overrules potential memories related to the mechanical object properties during intermanual transfer of grip and lift forces. Biomechanical properties of the object such as the weight do not seem to be used by the central nervous system as a first line information to evaluate grip force when handling an object or transferring information about the grasp to the opposite hemisphere. 4.1. Clinical implications Stroke or traumatic brain injury may cause an increased muscle tone, e.g. spasticity, or muscle contracture of the upper limb causing flexion deviation of the wrist within the horizontal plane (O’Dwyer et al., 1996; Pandyan et al., 2003). The overshoot in grip forces in relation to the lift forces to be observed at the affected hand after stroke has primarily been interpreted to reflect a strategy of the motor system to guarantee a stable grasp in the presence of sensorimotor dysfunction (McDonnell et al., 2006; Nowak et al., 2003). The changes in grip force scaling observed in stroke survivors might be influenced by deviation of the wrist in the horizontal plane, e.g. due to spasticity or contractures. Future studies should systematically address this issue. We found that the so-called sensorimotor memory used for intermanual transfer may be based on the motor commands used to handle an object rather than on the mechanical properties of the object. This observation may have an impact on rehabilitation techniques on stroke patients that make use of the unaffected hand to facilitate relearning of motor skills with the affected hand. The angulation of the wrist during training with the unaffected hand may influence the transfer of sensorimotor information to the affected hemisphere and potentially the motor skills to be produced with the affected hand. This should be taken into account when designing behavioral rehabilitation protocols focusing on hand motor control. Financial disclosures None of the authors has any financial disclosures regarding the present manuscript. Acknowledgements This work was supported by grants of the Deutsche Forschungsgemeinschaft (DFG, NO 737/5-1) and the Köln Fortune Programm (173/2006) to Dennis A. Nowak. Djamel Bensmail was supported by grants of Fondation Garches, SOFMER-IPSEN, Assistance Publique-Hôpitaux de Paris, Allergan and Medtronic. References Bensmail D, Sarfeld AS, Fink GR, Nowak DA. Sensorimotor processing in the grip-lift task: the impact of maximum wrist flexion/extension on force scaling. Clin Neurophysiol 2009;120:1588–95. Brenner E, Smeets JBJ. Size illusion influences how we lift but not how we grasp an object. Exp Brain Res 1996;111:473–6. Chang EC, Flanagan JR, Goodale MA. The intermanual transfer of anticipatory force control in precision grip lifting is not influenced by the perception of weight. Exp Brain Res 2008;185(2):319–29. Cole KJ. Lifting a familiar object: visual size analysis, not memory of object weight, scales lift force. Exp Brain Res 2008;188:551–7.
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