Abstract
Three experiments investigated the grip force exerted by the fingers on an object displaced actively in the near-body space. In one condition (unimanual) the object was held by one hand with the tripod grip and was moved briskly back and forth along one of the three coordinate directions (up–down, left–right, near–far). In the second condition (bimanual) the same point-to-point movements were performed while holding the object with the index and middle fingers of both hands. In the third condition (bimanual) the object was held as in the second condition and moved along a circular path lying in one of the three coordinate planes (horizontal, frontal, sagittal). In all conditions participants were asked to exert a baseline level of grip force largely exceeding the safety margin against slippage. Both grip forces and hand displacements were measured with high accuracy. As reported in previous studies, in the two point-to-point conditions we observed an upsurge of the grip force at the onset and at the end the movements. However, the timing of the transient increases of the grip force relative to hand kinematics did not confirm the hypothesis set forth by several previous studies that grip modulation is a pre-planned action based on an internal model of the expected effects of the movement. In the third condition, the systematic modulation of the grip force also for circular movements was again at variance with the internal model hypothesis because it cannot be construed as a pre-planned action aiming at countering large changes in dynamic load. We argue that a parsimonious account of the covariations of load and grip forces can be offered by taking into account the visco-elastic properties of the neuromuscular system.
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Notes
Note: In the relevant literature there are occasional terminological inconsistencies. Throughout this article we adopt the following terminology. Load force: total force acting on the manipulandum, i.e. the vector sum of the gravitational force and of the inertial force required to move. Grip force: total amount of force measured by the transducer along one axis. Following the convention adopted in robotics (Yoshikawa and Nagai 1991), grip force can be partitioned into two components: the inertial force vector aligned with the direction of the movement and the grasping force vector with which the manipulandum is held. The grasping force vector is aligned with the transducer axis along which stress is measured.
The sign convention in that figure is different from the one adopted here.
References
Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. Exp Brain Res Suppl 10:111–129
Bracewell RM, Wing AM, Soper HM, Clark KG (2003) Predictive and reactive co-ordination of grip and load forces in bimanual lifting in man. Eur J Neurosci 18:2396–2402
Burstedt MKO, Edin BB, Johansson RS (1997) Coordination of fingertip forces during human manipulation can emerge from independent neural networks controlling each engaged digit. Exp Brain Res 117:67–79
Cole KJ, Abbs JH (1988) Grip force adjustments evoked by load force perturbations of a grasped object. J Neurophysiol 60:1513–1522
Danion F, Sarlegna FR (2007) Can the human brain predict the consequences of arm movement corrections when transporting an object? Hints from grip force measurements. J Neurosci 27:12839–12843
Darainy M, Malfait N, Gribble PL, Towhidkhah F, Ostry DJ (2004) Learning to control arm stiffness under static condition. J Neurophysiol 92:3344–3350
Davidson PR, Wolpert DM (2005) Widespread access to predictive models in the motor system: a short review. J Neural Eng 2:S313–S319
Duque J, Thonnard JL, Vandermeeren Y, Sebire G, Cosnard G, Olivier E (2003) Correlation between impaired dexterity and corticospinal tract dysgenesis in congenital hemiplegia. Brain 126:732–747
Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis. Exp Brain Res 161:91–103
Feldman AG, Ostry DJ, Levin MF, Gribble PL, Mitnitski AB (1998) Recent tests of the equilibrium-point hypothesis (λ model). Mot Control 2:189–205
Flanagan JR, Tresilian JR (1994) Grip-load force coupling: a general control strategy for transporting objects. J Exp Psychol Hum Percept Perform 20:944–957
Flanagan JR, Wing AM (1993) Modulation of grip force with load force during point-to-point arm movements. Exp Brain Res 95:131–143
Flanagan JR, Wing AM (1995) The stability of precision grip forces during cyclic arm movements with a hand-held’975 load. Exp Brain Res 105:455–464
Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17:1519–1528
Flanagan JR, Tresilian JR, Wing AM (1993) Coupling of grip force and load during arm movements with grasped objects. Neurosci Lett 152:53–56
Flanagan JR, Tresilian JR, Wing AM (1995) Grip force adjustments during rapid hand movements suggest that detailed movement kinematics are predicted. Behav Brain Sci 18:753–754
Forssberg H, Eliasson AC, Redon-Zouitenn C, Nercuri E, Dubowitz L (1999) Impaired grip-lift synergy in children with unilateral brain lesions. Brain 122:1157–1168
Friedman J, Flash T (2007) Task-dependent selection of grasp kinematics and stiffness in human object manipulation. Cortex 43:444–460
Gao F, Latash ML, Zatsiorky VM (2005) Internal forces during object manipulation. Exp Brain Res 165:69–83
Gomi H, Osu R (1998) Task-dependent viscoelasticity of human multijoint arm and its spatial characteristics for interaction with environments. J Neurosci 18:8965–8978
Gordon AM, Duff SV (1999) Fingertip forces during object manipulation in children with hemiplegic cerebral palsy. I: anticipatory scaling. Dev Med Chil Neurol 41:166–175
Gorniak SL, Zatsiorsky VM, Latash LM (2010) Manipulation of a fragile object. Exp Brain Res 202:413–430
Grafton ST (2010) The cognitive neuroscience of prehension: recent developments. Exp Brain Res 204:475–491
Haggard P (1992) Multi-sensory control of motor control and learning. In: Summers JJ (ed) Approaches to the study of motor control and learning. Elsevier, New York, pp 195–231
Haggard P, Wing AM (1991) Responses to perturbation in human prehension. Neurosci Lett 122:103–108
Hu X, Murray WM, Perreult EJ (2012) Biomechanical constraints on the feedforward regulation of endpoint stiffness. J Neurophysiol 108:2083–2091
Iberall T, MacKenzie CL (1990) Opposition space and human prehension. In: Venkataraman ST, Iberall T (eds) Dextrous robot hands. Springer, New York, pp 32–54
Jakobson LS, Goodale MA (1991) Factors affecting higher-order movement planning. A kinematic analysis of human prehension. Exp Brain Res 86:199–208
Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A (eds) Attention and performance, vol 9. Erlbaum, Hillsdale, pp 153–168
Jeannerod M (1984) The timing of natural prehension movements. J Motor Behav 16:235–254
Jeannerod M (1986) The formation of finger grip during prehension. A cortically mediated visuomotor pattern. Behav Brain Res 19:99–116
Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320
Johansson RS (1991) How is grasping modified by Somatosensory input? In: Humphrey DG, Freund H-J (eds) Motor control: concepts and issues, Dahlem Konferenzen. Wiley, Chichester, pp 331–335
Johansson RS (1998) Sensory input and control of grip. In: Bock GR, Goode JA (eds) Novartis foundation symposium 218. Sensory guidance of movement. Wiley, Chicester, pp 45–63
Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564
Johansson RS, Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp Brain Res 66:141–154
Johansson RS, Westling C (1988) Programmed and triggered actions to rapid load changes during precision grip. Exp Brain Res 71:72–86
Johansson RS, Riso R, Häger C, Bäckström L (1992a) Somatosensory control of precision grip during unpredictable pulling loads. I. Changes in load force amplitude. Exp Brain Res 89:181–191
Johansson RS, Häger C, Riso R (1992b) Somatosensory control of precision grip during unpredictable pulling loads. II. Changes in load force rate. Exp Brain Res 89:192–203
Johansson RS, Häger C, Bäckström L (1992c) Somatosensory control of precision grip during unpredictable pulling loads. III. Impairments during digital anesthesia. Exp Brain Res 89:204–213
Kinoshita H, Ikuta K, Kawai S, Udo M (1993) Effects of lifting speed and height on the regulation of forces during lifting tasks using a precision grip. J Hum Mov Stud 25:151–175
Kinoshita H, Ikuta K, Kawai S, Teraoka T (1995) Individual finger forces acting on a grasped object during shaking actions. Ergonomics 39:243–256
Macefield VG, Häger-Ross C, Johansson RS (1996) Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp Brain Res 108:155–171
Martin JB, Chaffin DB (1972) Biomechanical computerized simulation of human strength in sagittal-plane activities. AIIE Trans 4:19–28
Ogden C, Fryar C, Carroll M, Flegal K (2004) Mean body weight, height, and body mass index, United States 1960–2002. Adv Data 347:1–17
Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1990) The coupling of arm and finger movements during prehension. Exp Brain Res 79:431–435
Perreault EJ, Kirsch RF, Crago PE (2002) Voluntary control of static endpoint stiffness during force regulation tasks. J Neurophysiol 87:2808–2816
Pilon J-F, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67
Raghavan P, Krakauer JW, Gordon AM (2006) Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunal syndrome. Brain 129:1415–1425
Serrien DJ, Wiesendanger M (2001a) Dissociation of grp/load force coupling during a bimanual manipulative assignment. Exp Brain Res 136:417–420
Serrien DJ, Wiesendanger M (2001b) Bimanual organization of manipulative force: evidence from erroneous feedforward programming of precision grip. Eur J Neurosci 13:153–160
Slota GP, Latash ML, Zatsiorsky VM (2011) Grip forces during object manipulation: experiment, mathematical model, and validation. Exp Brain Res 213:125–139
Smith MA, Soetching JF (2005) Modulation of grasping forces during object transport. J Neurophysiol 93:137–145
Stucchi N, Viviani P (1993) Cerebral dominance and asynchrony between bimanual two-dimensional movements. J Exp Psychol HPP 19:1200–1220
von Hofsten C, Rönnqvist L (1988) Preparation for grasping an object: a developmental study. J Exp Psychol Hum Percept Perform 14:610–621
Wallace SA, Weeks DL (1989) Temporal constraints in the control of prehensile movement. J Mot Behav 20:81–105
Winges SA, Soechting JF, Flanders M (2007) Multidigit control of contact forces during transport of handheld objects. J Neurophysiol 98:851–860
Witney AG, Wolpert DM (2007) The effects of externally generated loading on predictive grip force modulation. Nerosci Lett 414:10–15
Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732
Yang JF, Scholz JP, Latash ML (2007) The role of kinematic redundancy in adaptation of reaching. Exp Brain Res 176:54–69
Yoshikawa T, Nagai K (1991) Manipulating and grasping forces in manipulation by multifingered robot hands. IEEE Trans Robot Autom 7:67–77
Zatsiorky VM, Latash ML (2008) Multifinger prehension: an overview. J Mot Behav 40:446–476
Zatsiorsky VM, Gao F, Latash ML (2005) Motor control goes beyond physics: differential effects of gravity and inertia on finger forces during manipulation of hand-held objects. Exp Brain Res 162:300–308
Acknowledgments
We thank Dr. Mauro Carrozzo for help with the experiments and Prof. Andrea d’Avella for providing the force transducer. The work was supported by the Italian Ministry of University and Research (PRIN Grant 2010MEFNF7_002) and Italian Space Agency (COREA Grant).
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Appendix
Appendix
We describe a simple mechanical model for simulating the experimental results. The central assumption is that the end-point position P is determined by the opposing forces generated by two mass-spring systems, where the springs have constant stiffness K and controllable resting lengths L 0 (Fig. 10a). Displacements of the end-point position P are generated by modulating appropriately the resting lengths. The scheme described here applies directly to the case where movement and grip forces are aligned. When they are not aligned (e.g., for vertical point-to-point movements) we assume that two such schemes are at work, one responsible for the displacement, the other for holding the manipulandum. Thus, as argued in the Discussion, the grip modulations measured in the holding scheme—within which the frame is not moving—are the indirect reflection of the modulations occurring in the moving scheme. A similar assumption is made in the case of circular motions where the role of the two schemes switches every half-period of the motion.
The system is depicted in Fig. 10b. A mass M moves under the joint pull of the springs with stiffness K 1 and K 2. The outer ends of the springs are attached at a fixed distance L from the 0 reference and time-varying resting length L 01(t) and L 02(t). Motion is damped by a linear viscous damper with coefficient C. The input to the system are the effective lengths of the springs, defined as X 1(t) = L − L 01(t) and X 2(t) = L − L 02(t). The equation of the motion is:
where x(t) is the signed distance of the mass for the 0 reference. Because of the way the springs are attached, the grip force acting on the mass during the motion is: G f(t) = K 1 X 1(t) + K 2 X 2(t) + x(t)·(K 2 − K 1).
To simulate the results for point-to-point linear movements, X 1(t) and X 2(t) were modeled by two sequences of low-pass-filtered pulses with the same period (T = 2.4 s), amplitude and baseline, each modulating in opposite directions the force exerted by the springs. The leading and trailing edges of the pulses were modeled by generalized sigmoid functions:
Figure 11 shows a normalized representation of the individual pulses X 1(t) and X 2(t) (baseline not shown). We assumed K 1 = K 2. Thus, the grip force is proportional to the sum X 1(t) + X 2(t), which is also shown in the upper part of the figure. In this scheme grip modulations emerge from the overlap between the leading edge of a pulse and the trailing edge of the previous pulse pulling in the opposite direction. Pulse amplitude and baseline were set to reproduce the average grip force and the prescribed displacement amplitude (40 cm). The grip force time course was simulated by choosing appropriately the slope difference for pulses in opposite directions. The kinematics of the mass was obtained by solving the equation of the motion with the best-fitting parameters M, C and K (see below). Figure 12 compares the simulation with the actual data in the case of transversal U-grip motions (see Fig. 2) where the peaks of the grip force (upper panel) and the acceleration profiles (lower panel) in the two phases of the movement were significantly different.
The model behavior was also compared with the results for the two main components of circular movements. We assumed that movement trajectories are generated by a combination of two mechanical systems as the one in Fig. 10b acting along orthogonal axes. For one system the effective lengths vary as X 1(t) = A x sin(ωt) + B x and X 2(t) = A x sin(ωt + θ x ) + B x . For the orthogonal system they vary as Y 1(t) = A y cos(ωt) + B y and Y 2(t) = A y cos(ωt + θ y ) + B y (ω = 2π/T). Thus, for the X-axis, the driving force K 1 X 1 − K 2 X 2 is an harmonic function F sin(ωt + ψ) where
As in the case of rectilinear movements, grip forces emerge because the phase difference θ produces a partial overlap between the components K 1 X 1 and K 2 K 2 of the driving force. The experimental results were simulated by making again for each axis separately the simplifying assumption K 1 = K 2 = K, so that the grip force is GF(t) = K(X 1 + X 2) = Gsin(ωt + φ) where
Because trajectories were not perfectly circular, the amplitude parameter A was estimated independently for each axis from the data. Then, we determined the model parameters affording the best fit to both the actual grip force profile and to the kinematics of the movement. Figure 13 compares experimental and simulated data in the case of the X-axis for movements in the frontal (X–Y) plane. The approximation was equally good for the Y axis in the frontal plane and for both X- and Z-axis for movements in the horizontal plane. Our scheme assumes that movements were strictly planar. Therefore, it cannot account for grip modulations measured in the sagittal plane (Figs. 8c, 9c), which may in part reflect the significant deviations of the movement from planarity.
The driving force is proportional to the stiffness K. Thus, in fitting the simulation to the data only the ratios C/M and K/M can be specified independently. However, we verified that the stiffness values required to mimic grip forces in linear and circular movements are at least realistic. From the average body mass for individuals in the age range of the participants (M b = 78.24 kg, Ogden et al. 2004), and the average ratio between arm and body mass (M a /M b = 0.062, Martin and Chaffin 1972), one obtains: M a = 4.85 kg. For linear U-grip movements, the fitting shown in Fig. 12 required a ratio K/M = 138.9, yielding an estimated stiffness K = 6736 N/m. The required ratio C/M = 9.69 yielded the estimate C = 470 N s/m. For circular movements (Fig. 13) the fitting required K/M = 55.56 and C/M = 8.33. Because both arms were involved, we assumed that the moving mass was twice as large as in single arm movements. This yielded an estimated equivalent stiffness K = 5384 N/m and an estimated equivalent viscosity C = 808 N s/m. Though approximate, stiffness estimates are well in keeping with those reported by Hu et al. (2012) for maximally stiffened arms in the horizontal plane.
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Viviani, P., Lacquaniti, F. Grip forces during fast point-to-point and continuous hand movements. Exp Brain Res 233, 3201–3220 (2015). https://doi.org/10.1007/s00221-015-4388-4
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DOI: https://doi.org/10.1007/s00221-015-4388-4