Abstract
The goal of this study was to elucidate the underlying mechanisms of hand and tool grasping control. We assumed that there is a single principle-governing grasping control irrespective of its effectors and that the degree of prior experience of the effector determines the smoothness of aperture control. Eight participants performed a reach-to-grasp task with four different effectors: index finger and thumb, middle finger and thumb, chopsticks, and a scissor-like tool. Although we employed different effectors with large mechanical variations and different degrees of prior use, maximum grip aperture was scaled as a function of object size and appeared at almost the same timing in all four types of grasping movements. Moreover, reaching time did not substantially differ among grasping conditions. However, plateau duration of the aperture profile differed by effector. Plateau duration was the longest in the unfamiliar scissor-like tool grasping condition. There was no difference between the unfamiliar hand-use grasp with the thumb and the middle finger and the familiar tool-grasp with chopsticks. The familiar hand-use grasp with the thumb and the index finger had the shortest plateau duration. These results supported the idea that there is an effector-independent continuity between hand-use and tool-use in motor control as a function of prior degree of use, rather than the conventionally assumed dichotomy between them.
Similar content being viewed by others
References
Adamovich SV, Archambault PS, Ghafouri M, Levin MF, Poizner H, Feldman AG (2001) Hand trajectory invariance in reaching movements involving the trunk. Exp Brain Res 138:288–303
Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. In: Goodwin AW, DarianSmith I (eds) Hand function and the neocortex, pp 111–129
Berti A, Frassinetti F (2000) When far becomes near: remapping of space by tool use. J Cogn Neurosci 12:415–420
Bhushan N, Shadmehr R (1999) Computational nature of human adaptive control during learning of reaching movements in force fields. Biol Cybern 81:39–60
Bongers RM (2010) Do changes in movements after tool use depend on body schema or motor learning? In Haptics: generating and perceiving tangible sensations. Springer Berlin Heidelberg, pp 271–276
Bongers RM, Zaal FT, Jeannerod M (2012) Hand aperture patterns in prehension. Hum Mov Sci 31:487–501
Bouwsema H, der Sluis CKV, Bongers RM (2010) Movement characteristics of upper extremity prostheses during basic goal-directed tasks. Clin Biomech 25:523–529
Brozzoli C, Cardinali L, Pavani F, Farnè A (2010) Action-specific remapping of peripersonal space. Neuropsychologia 48:796–802
Brozzolli C, Pavani F, Urquizar C, Cardinali L, Farne A (2009) Grasping action remap peripersonal space. Neuroreport 20:913–917
Burdet E, Osu R, Franklin DW, Milner TE, Kawato M (2001) The central nervous system stabilizes unstable dynamics by learning optimal impedance. Nature 414:446–449
Cardinali L, Frassinetti F, Brozzoli C, Urquizar C, Roy AC, Farnè A (2009) Tool-use induces morphological updating of the body schema. Curr Biol 19:R478–R479
Darainy M, Malfait N, Gribble PL, Towhidkhah F, Ostry DJ (2004) Learning to control arm stiffness under static conditions. J Neurophysiol 92:3344–3350
De Vignemont F, Farnè A (2010) Widening the body to rubber hands and tools: what’s the difference? Rev Neuropsychol 2:203–211
Farnè A, Làdavas E (2000) Dynamic size-change of hand peripersonal space following tool use. Neuroreport 11:1645–1649
Flanagan JR, Johansson RS (2003) Action plans used in action observation. Nature 424:769–771
Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5:1688–1703
Franklin DW, Milner TE (2003) Adaptive control of stiffness to stabilize hand position with large loads. Exp Brain Res 152:211–220
Gentili R, Han CE, Schweighofer N, Papaxanthis C (2010) Motor learning without doing: trial-by-trial improvement in motor performance during mental training. J Neurophysiol 104:774–783
Gentilucci M, Roy AC, Stefanini S (2004) Grasping an object naturally or with a tool: are these tasks guided by a common motor representation? Exp Brain Res 157:496–506
Grosskopf A, Kuhtz-Buschbeck JP (2006) Grasping with the left and right hand: a kinematic study. Exp Brain Res 168:230–240
Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784
Hoff B, Arbib MA (1993) Models of trajectory formation and temporal interaction of reach and grasp. J Mot Behav 25:175–192
Ingram JN, Körding KP, Howard IS, Wolpert DM (2008) The statistics of natural hand movements. Exp Brain Res 188:223–236
Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7:2325–2330
Itaguchi Y, Fukuzawa K (2012a) Effects of arm stiffness and muscle effort on position reproduction error in the horizontal plane. Percept Mot Skills 114:757–773
Itaguchi Y, Fukuzawa K (2012b) The influence of the indicator arm on end point distribution in proprioceptive localization with multi-joint arms. Exp Brain Res 222:77–88
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 (1984) The timing of natural prehension movements. J Mot Behav 16:235–254
Jeannerod M (1988) The neural and behavioural organization of goal-directed movements. Clarendon Press/Oxford University Press
Kaminski TR, Bock C, Gentile AM (1995) The coordination between trunk and arm motion during pointing movements. Exp Brain Res 106:457–466
Kao KLC, Goodale MA (2009) Enhanced detection of visual targets on the hand and familiar tools. Neuropsychol 47:2454–2463
Kawato M, Wolpert D (1998) Internal models for motor control. In: Sensory guidance of movement (Novartis Foundation Symposium 218), Wiley, Chichester, pp 291–307
Malfait N, Ostry DJ (2004) Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24:8084–8089
Maravita A, Iriki A (2004) Tools for the body (schema). Trends Cogn Sci 8:79–86
Maravita A, Clarke K, Husain M, Driver J (2002a) Active tool use with the contralesional hand can reduce cross-modal extinction of touch on that hand. Neurocase 8:411–416
Maravita A, Spence C, Kennett S, Driver J (2002b) Tool-use changes multimodal spatial interactions between vision and touch in normal humans. Cognition 83:B25–B34
Meulenbroek RG, Rosenbaum DA, Jansen C, Vaughan J, Vogt S (2001) Multijoint grasping movements. Exp Brain Res 138:219–234
Napier JR (1956) The prehensile movements of the human hand. J Bone Joint Surg 38:902–913
Osiurak F, Jarry C, Le Gall D (2011) Re-examining the gesture engram hypothesis. New perspectives on apraxia of tool use. Neuropsychologia 49:299–312
Rosenbaum DA, Meulenbroek RG, Vaughan J, Jansen C (2001) Posture-based motion planning: applications to grasping. Psychol Rev 108:709–734
Smeets JB, Brenner E (1999) A new view on grasping. Mot Control 3:237–271
Tresilian JR, Stelmach GE, Adler CH (1997) Stability of reach-to-grasp movement patterns in Parkinson’s disease. Brain 120:2093–2111
Umiltà MA, Intskirveli I, Grammont F et al (2008) When pliers become fingers in the monkey motor system. PNAS 105:2209–2213
Uno Y, Kawato M, Suzuki R (1989) Formation and control of optimal trajectory in human multijoint arm movement. Biol Cybern 61:89–101
Wang J, Stelmach GE (1998) Coordination among the body segments during reach-to-grasp action involving the trunk. Exp Brain Res 123:346–350
Williams A, Gribble PL (2012) Observed effector-independent motor learning by observing. J Neurophysiol 107:1564–1570
Wing AM, Fraser C (1983) The contribution of the thumb to reaching movements. Q J Exp Psychol 35:297–309
Witt JK, Proffitt DR, Epstein W (2005) Tool use affects perceived distance, but only when you intend to use it. J Exp Psychol Hum Percept Perform 31:880–888
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Itaguchi, Y., Fukuzawa, K. Hand-use and tool-use in grasping control. Exp Brain Res 232, 3613–3622 (2014). https://doi.org/10.1007/s00221-014-4053-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-014-4053-3