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Asymmetry in grasp force matching and sense of effort

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Abstract

While asymmetries in upper limb force matching have been observed, the mechanisms underlying asymmetry in the sense of effort have not been conceptualized. The aim of this study was to investigate asymmetries in the perception and reproduction of grasp force. Forty-two young adults, 22 right-handed (RH) and 20 left-handed (LH), were, respectively, divided into three groups according to differences between their right and left-hand strength (left stronger than right, right stronger than left and right & left equivalent). A reference force, representing 20% of the maximal voluntary contraction (MVC) produced by the right or left hand, was matched with same hand (Ipsilateral Remembered—IR) or opposite (Contralateral Remembered—CR) hand. The matching relative error was 92% (for RH) and 46% (for LH) greater in the CR than IR condition. Asymmetries in matching were significant for RH participants only in the CR condition and were dependent on right/left differences in hand strength as shown by the constant error (CE). For this RH population, right-hand overshoot of the left-hand reference and left-hand undershoot of the right-hand reference were significant when the right hand was stronger than the left. Asymmetry remained significant when CE was normalized (%MVC). Asymmetry was reduced when the strength of each hand was equivalent or when the left hand was stronger than the right. These findings suggest that effort perception is asymmetric in RH but not in LH individuals. The hand x strength interaction indicates that asymmetry in force matching is a consequence of both a difference in the respective cortical representations and motor components, which confer a different “gain” (input–output relationship) to each system. The similarity with position sense asymmetry suggests that the gain concept may be generalized to describe some functional/performance differences between the two hand/hemisphere systems. The more symmetrical performance of the LH than RH group underlines that context specific influence of handedness, hemisphere dominance and hemispheric interactions modulate performance symmetries/asymmetries.

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References

  • Adamo DE, Martin BJ (2009) Position sense asymmetry. Exp Brain Res 192:87–95

    Article  PubMed  Google Scholar 

  • Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE, Zilles K (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4:216–222

    Article  PubMed  CAS  Google Scholar 

  • Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38:304–312

    Article  PubMed  CAS  Google Scholar 

  • Babiloni C, Carducci F, Del Gratta C, Demartin M, Romani GL, Babiloni F, Rossini PM (2003) Hemispherical asymmetry in human SMA during voluntary simple unilateral movements. An fMRI study. Cortex 39:293–305

    Article  PubMed  Google Scholar 

  • Baraldi P, Porro CA, Serafini M, Pagnoni G, Murari C, Corazza R, Nichelli P (1999) Bilateral representation of sequential finger movements in human cortical areas. Neurosci Lett 269:95–98

    Article  PubMed  CAS  Google Scholar 

  • Bernard JA, Taylor SF, Seidler RD (2011) Handedness, dexterity, and motor cortical representations. J Neurophysiol 105:88–99

    Article  PubMed  Google Scholar 

  • Blatow M, Nennig E, Durst A, Sartor K, Stippich C (2007) fMRI reflects functional connectivity of human somatosensory cortex. Neuroimage 37:927–936

    Article  PubMed  Google Scholar 

  • Brouwer B, Sale MV, Nordstrom MA (2001) Asymmetry of motor cortex excitability during a simple motor task: relationships with handedness and manual performance. Exp Brain Res 138:467–476

    Article  PubMed  CAS  Google Scholar 

  • Cafarelli E, Bigland-Ritchie B (1979) Sensation of static force in muscles of different length. Exp Neurol 65:511–525

    Article  PubMed  CAS  Google Scholar 

  • Cafarelli E, Kostka CE (1981) Effect of vibration on static force sensation in man. Exp Neurol 74:331–340

    Article  PubMed  CAS  Google Scholar 

  • Carson RG, Riek S, Shahbazpour N (2002) Central and peripheral mediation of human force sensation following eccentric or concentric contractions. J Physiol 539:913–925

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Gerloff C, Hallett M, Cohen LG (1997) Involvement of the ipsilateral motor cortex in finger movements of different complexities. Ann Neurol 41:247–254

    Article  PubMed  CAS  Google Scholar 

  • Cherbuin N, Brinkman C (2006) Hemispheric interactions are different in left-handed individuals. Neuropsychology 20:700–707

    Article  PubMed  Google Scholar 

  • Crago PE, Houk JC, Rymer WZ (1982) Sampling of total muscle force by tendon organs. J Neurophysiol 47:1069–1083

    PubMed  CAS  Google Scholar 

  • Cykowski MD, Coulon O, Kochunov PV, Amunts K, Lancaster JL, Laird AR, Glahn DC, Fox PT (2008) The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. Cereb Cortex 18:1999–2009

    Article  PubMed  Google Scholar 

  • Franz EA, Rowse A, Ballantine B (2002) Does handedness determine which hand leads in a bimanual task? J Mot Behav 34:402–412

    Article  PubMed  Google Scholar 

  • Gandevia SC (1982) The perception of motor commands or effort during muscular paralysis. Brain 105:151–159

    Article  PubMed  CAS  Google Scholar 

  • Gandevia SC, McCloskey DI (1977) Changes in motor commands, as shown by changes in perceived heaviness, during partial curarization and peripheral anaesthesia in man. J Physiol 272:673–689

    PubMed  CAS  Google Scholar 

  • Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas CK (1995) Neurobiology of muscle fatigue. Advances and issues. Adv Exp Med Biol 384:515–525

    PubMed  CAS  Google Scholar 

  • Goble D, Noble BC, Brown SH (2009) Proprioceptive target matching asymmetries in left-handed individuals. Exp Brain Res 197:403–408

    Article  PubMed  Google Scholar 

  • Gordon AM, Forssberg H, Iwasaki N (1994) Formation and lateralization of internal representations underlying motor commands during precision grip. Neuropsychologia 32:555–568

    Article  PubMed  CAS  Google Scholar 

  • Haaland KY (2006) Left hemisphere dominance for movement. Clin Neuropsychol 20:609–622

    Article  PubMed  Google Scholar 

  • Halsband U, Ito N, Tanji J, Freund HJ (1993) The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain J Neurol 116(Pt 1):243–266

    Article  Google Scholar 

  • Haude RH, Morrow-Tlucak M, Fox DM, Pickard KB (1987) Differential visual field-interhemispheric transfer: can it explain sex and handedness differences in lateralization? Percept Mot Skills 65:423–429

    Article  PubMed  CAS  Google Scholar 

  • Henningsen H, Ende-Henningsen B, Gordon AM (1995) Asymmetric control of bilateral isometric finger forces. Exp Brain Res 105:304–311

    PubMed  CAS  Google Scholar 

  • Incel N, Ceceli E, Durukan P, Erdem H, Yorgancioglu Z (2002) Grip strength: effect of hand dominance. Singapore Med J 43(5):234–237

    PubMed  Google Scholar 

  • Jagacinski R, Flach J (2003) Control theory for humans: quantitative approaches to modeling performance. Lawrence Erlbaum Associates, London

  • Jami L (1992) Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiol Rev 72:623–666

    PubMed  CAS  Google Scholar 

  • Johansson RS, Cole KJ (1992) Sensory-motor coordination during grasping and manipulative actions. Curr Opin Neurobiol 2:815–823

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jones LA (1986) Perception of force and weight: theory and research. Psychol Bull 100:29–42

    Article  PubMed  CAS  Google Scholar 

  • Jones L (1989) Force matching by patients with unilateral focal cerebral lesions. Neuropsychologia 27:1153–1163

    Article  PubMed  CAS  Google Scholar 

  • Jones LA (2003) Perceptual constancy and the perceived magnitude of muscle forces. Exp Brain Res 151:197–203

    Article  PubMed  Google Scholar 

  • Jones LA, Hunter IW (1982) Force sensation in isometric contractions: a relative force effect. Brain Res 244:186–189

    Article  PubMed  CAS  Google Scholar 

  • Jones LA, Hunter IW (1983) Effect of fatigue on force sensation. Exp Neurol 81:640–650

    Article  PubMed  CAS  Google Scholar 

  • Jones LA, Piateski E (2006) Contribution of tactile feedback from the hand to the perception of force. Exp Brain Res 168:298–302

    Article  PubMed  Google Scholar 

  • Jung P, Baumgartner U, Bauermann T, Magerl W, Gawehn J, Stoeter P, Treede RD (2003) Asymmetry in the human primary somatosensory cortex and handedness. Neuroimage 19:913–923

    Article  PubMed  Google Scholar 

  • Jung P, Baumgartner U, Magerl W, Treede RD (2008) Hemispheric asymmetry of hand representation in human primary somatosensory cortex and handedness. Clin Neurophysiol 119:2579–2586

    Article  PubMed  Google Scholar 

  • Kilbreath SL, Gandevia SC, Wirianski A, Hewitt B (1995) Human flexor pollicis longus: role of peripheral inputs in weight-matching. Neurosci Lett 201:203–206

    Article  PubMed  CAS  Google Scholar 

  • Kim SG, Ashe J, Hendrich K, Ellermann JM, Merkle H, Ugurbil K, Georgopoulos AP (1993) Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science 261:615–617

    Article  PubMed  CAS  Google Scholar 

  • Klöppel S, van Eimeren T, Glauche V, Vongerichten A, Munchau A, Frackowiak RSJ, Buchel C, Weiller C, Siebner HR (2007a) The effect of handedness on cortical motor activation during simple bilateral movements. NeuroImage 34:274–280

    Article  PubMed  Google Scholar 

  • Klöppel S, Vongerichten A, van Eimeren T, Frackowiak RS, Siebner HR (2007b) Can left-handedness be switched? Insights from an early switch of handwriting. J Neurosci Official J Soc Neurosci 27:7847–7853

    Article  Google Scholar 

  • Lafargue G, Sirigu A (2006) The nature of the sense of effort and its neural substrate. Rev Neurol (Paris) 162:703–712

    Article  CAS  Google Scholar 

  • Lafargue G, Paillard J, Lamarre Y, Sirigu A (2003) Production and perception of grip force without proprioception: is there a sense of effort in deafferented subjects? Eur J Neurosci 17:2741–2749

    Article  PubMed  Google Scholar 

  • Lafargue G, Franck N, Sirigu A (2006) Sense of motor effort in patients with schizophrenia. Cortex 42:711–719

    Article  PubMed  Google Scholar 

  • Li S (2006) Perception of individual finger forces during multi-finger force production tasks. Neurosci Lett 409:239–243

    Article  PubMed  CAS  Google Scholar 

  • Martin K, Jacobs S, Frey SH (2011) Handedness-dependent and -independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning. Neuroimage 57:502–512

    Article  PubMed  Google Scholar 

  • Marzi CA, Bisiacchi P, Nicoletti R (1991) Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia 29:1163–1177

    Article  PubMed  CAS  Google Scholar 

  • McCloskey DI (1974) Muscular and cutaneous mechanisms in the estimation of the weights of grasped objects. Neuropsychologia 12:513–520

    Article  PubMed  CAS  Google Scholar 

  • Nihashi T, Naganawa S, Sato C, Kawai H, Nakamura T, Fukatsu H, Ishigaki T, Aoki I (2005) Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation—an fMRI study. Clin Neurophysiol 116:842–848

    Article  PubMed  Google Scholar 

  • Nowak DA, Hermsdorfer J (2003) Selective deficits of grip force control during object manipulation in patients with reduced sensibility of the grasping digits. Neurosci Res 47:65–72

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Park WH, Leonard CT (2008) The effect of intervening forces on finger force perception. Neurosci Lett 438:286–289

    Article  PubMed  CAS  Google Scholar 

  • Park WH, Leonard CT, Li S (2007) Perception of finger forces within the hand after index finger fatiguing exercise. Exp Brain Res 182:169–177

    Article  PubMed  Google Scholar 

  • Park WH, Leonard CT, Li S (2008) Finger force perception during ipsilateral and contralateral force matching tasks. Exp Brain Res 189:301–310

    Article  PubMed  Google Scholar 

  • Petersen P, Petrick M, Connor H, Conklin D (1989) Grip strength and hand dominance: challenging the 10% rule. Am J Occup Therapy 43:444–447

    CAS  Google Scholar 

  • Robinson LM, Fitts SS, Kraft GH (1990) Laterality of performance in fingertapping rate and grip strength by hemisphere of stroke and gender. Arch Phys Med Rehabil 71:695–698

    PubMed  CAS  Google Scholar 

  • Rushworth MF, Johansen-Berg H, Gobel SM, Devlin JT (2003) The left parietal and premotor cortices: motor attention and selection. Neuroimage 20 Suppl 1: S89-100

  • Sainburg RL (2005) Handedness: differential specializations for control of trajectory and position. Exerc Sport Sci Rev 33:206–213

    Article  PubMed  Google Scholar 

  • Schaefer SY, Haaland KY, Sainburg RL (2007) Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. Brain 130:2146–2158

    Article  PubMed  Google Scholar 

  • Shen YC, Franz EA (2005) Hemispheric competition in left-handers on bimanual reaction time tasks. J Mot Behav 37:3–9

    Article  PubMed  Google Scholar 

  • Shergill SS, Bays PM, Frith CD, Wolpert DM (2003) Two eyes for an eye: the neuroscience of force escalation. Science 301:187

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Limmer C, Peinemann A, Drzezga A, Bloem BR, Schwaiger M, Conrad E (2002) Long-term consequences of switching handedness: a positron emission tomography study on handwriting in “converted” left-handers. J Neurosci 22:2816–2825

    PubMed  CAS  Google Scholar 

  • Singh LN, Higano S, Takahashi S, Kurihara N, Furuta S, Tamura H, Shimanuki Y, Mugikura S, Fujii T, Yamadori A, Sakamoto M, Yamada S (1998) Comparison of ipsilateral activation between right and left handers: a functional MR imaging study. Neuroreport 9:1861–1866

    Article  PubMed  CAS  Google Scholar 

  • Soros P, Knecht S, Imai T, Gurtler S, Lutkenhoner B, Ringelstein EB, Henningsen H (1999) Cortical asymmetries of the human somatosensory hand representation in right- and left-handers. Neurosci Lett 271:89–92

    Article  PubMed  CAS  Google Scholar 

  • Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104:542–550

    Article  PubMed  Google Scholar 

  • Toffin D, McIntyre J, Droulez J, Kemeny A, Berthoz A (2003) Perception and reproduction of force direction in the horizontal plane. J Neurophysiol 90:3040–3053

    Article  PubMed  CAS  Google Scholar 

  • Triggs WJ, Subramanium B, Rossi F (1999) Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation. Brain Res 835:324–329

    Article  PubMed  CAS  Google Scholar 

  • van den Berg FE, Swinnen SP, Wenderoth N (2010) Hemispheric asymmetries of the premotor cortex are task specific as revealed by disruptive TMS during bimanual versus unimanual movements. Cereb Cortex 20:2842–2851

    Article  PubMed  Google Scholar 

  • van den Berg FE, Swinnen SP, Wenderoth N (2011) Involvement of the primary motor cortex in controlling movements executed with the ipsilateral hand differs between left- and right-handers. J Cogn Neurosci, http://www.mitpressjournals.org/doi/abs/10.1162/jocn_a_00018?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed. Accessed 10 September 2011

  • Verstynen T, Diedrichsen J, Albert N, Aparicio P, Ivry RB (2005) Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol 93:1209–1222

    Article  PubMed  Google Scholar 

  • Volkmann J, Schnitzler A, Witte OW, Freund H (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79:2149–2154

    PubMed  CAS  Google Scholar 

  • Wang J, Sainburg RL (2006) Interlimb transfer of visuomotor rotations depends on handedness. Exp Brain Res 175:223–230

    Article  PubMed  Google Scholar 

  • Wegner K, Forss N, Salenius S (2000) Characteristics of the human contra- versus ipsilateral SII cortex. Clin Neurophysiol 111:894–900

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski AB (1998) Sexually-dimorphic patterns of cortical asymmetry, and the role for sex steroid hormones in determining cortical patterns of lateralization. Psychoneuroendocrinology 23:519–547

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi M, Imanaka K, Nakayama M, Nishizawa S (2004) Lateral difference and interhemispheric transfer on arm-positioning movement between right and left handers. Percept Mot Skills 98:1199–1209

    PubMed  Google Scholar 

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Acknowledgments

Faculty Research Award I, II, Eugene Applebaum College of Pharmacy and Health Sciences, Wayne State University awarded to D.E. Adamo. Support from the Eugene Applebaum College of Pharmacy and Health Sciences, Wayne State University to S Scotland, University of Michigan. Special thanks to Rajiv George, Movement Analysis and Performance Sciences Laboratory, Wayne State University for his assistance with data collection and processing. Special thanks to E. Claxton and C. Woolley, Industrial and Operations Engineering University of Michigan for designing the grasp force instrumentation.

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Correspondence to Diane E. Adamo.

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Adamo, D.E., Scotland, S. & Martin, B.J. Asymmetry in grasp force matching and sense of effort. Exp Brain Res 217, 273–285 (2012). https://doi.org/10.1007/s00221-011-2991-6

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