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Hard and fast rules about the body: contributions of the action stream to judging body space

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Abstract

Analogously to the visual system, somatosensory processing may be segregated into two streams, with the body constituting either part of the action system or a perceptual object. Experimental studies with participants free from neurological disease which test this hypothesis are rare, however. The present study explored the contributions of the two putative streams to a task that requires participants to estimate the spatial properties of their own body. Two manipulations from the visuospatial literature were included. First, participants were required to point either backward towards pre-defined landmarks on their own body (egocentric reference frame) or to a forward projection of their own body (allocentric representation). Second, a manipulation of movement mode was included, requiring participants to perform pointing movements either immediately, or after a fixed delay, following instruction. Results show that accessing an allocentric representation of one’s own body results in performance changes. Specifically, the spatial bias shown to exist for body space when pointing backward at one’s own body disappears when participants are requested to mentally project their body to a pre-defined location in front space. Conversely, delayed execution of pointing movements does not result in performance changes. Altogether, these findings provide support for a constrained dual stream hypothesis of somatosensory processing and are the first to show similarities in the processing of body space and peripersonal space.

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References

  • Anema HA, van Zandvoort MJE, De Haan EHF, Kappelle LJ, de Kort PLM, Jansen BPW, Dijkerman HC (2009) A double dissociation between somatosensory processing for perception and action. Neuropsychologia 47:1615–1620

    Article  PubMed  Google Scholar 

  • Atkeson CG, Hollerbach JM (1985) Kinematic features of unrestrained vertical arm movements. J Neurosci 5:2318–2330

    PubMed  CAS  Google Scholar 

  • Bagesteiro LB, Sainburg RL (2002) Handedness: dominant arm advantages in control of limb dynamics. J Neurophysiol 88:2408–2421

    Article  PubMed  Google Scholar 

  • Bisiach E, McIntosh RD, Dijkerman HC, McClements KI, Colombo M, Milner AD (2004) Visual and tactile length matching in spatial neglect. Cortex 40:651–657

    Article  PubMed  Google Scholar 

  • Blanke O, Landis T, Spinelli L, Seeck M (2004) Out-of-body experience and autoscopy of neurological origin. Brain 127:243–258

    Article  PubMed  Google Scholar 

  • Blanke O, Mohr C, Michel CM et al (2005) Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction. J Neurosci 25:550–557

    Article  PubMed  CAS  Google Scholar 

  • Bottini G, Bisiach E, Sterzi R, Vallar G (2002) Feeling touches in someone else’s hand. Neuroreport 13:249–252

    Article  PubMed  Google Scholar 

  • Carson RG, Elliott D, Goodman D, Chua R (1993) Asymmetries in the regulation of visually guided aiming. J Motor Behav 25:21–32

    Article  CAS  Google Scholar 

  • Christman SD, Bentle M, Niebauer CL (2007) Handedness differences in body image distortion and eating disorder symptomatology. Int J Eat Disord 40:247–256

    Article  PubMed  Google Scholar 

  • Cohen NR, Cross ES, Tunik E, Grafton ST, Culham JC (2009) Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: a TMS approach. Neuropsychologia 47:1553–1562

    Article  PubMed  Google Scholar 

  • Committeri G, Pitzalis S, Galati G et al (2007) Neural bases of personal and extrapersonal neglect in humans. Brain 130:431–441

    Article  PubMed  Google Scholar 

  • De Vignemont F, Tsakiris M, Haggard P (2005) Body mereology. In: Knoblich G, Thornton IM, Grosjean M, Shiffrar M (eds) Human body perception from the inside out. Oxford University Press, New York, pp 147–170

    Google Scholar 

  • Desmurget M, Prablanc C, Jordan M, Jeannerod M (1999) Are reaching movements planned to be straight and invariant in the extrinsic space? Kinematic comparisons between compliant and unconstrained motions. Q J Exp Psychol 52 A:981–1020

    Article  Google Scholar 

  • Desmurget M, Gaveau V, Vindras P, Turner RS, Broussolle E, Thobois S (2004) On-line motor control in patients with Parkinson’s disease. Brain 127:1755–1773

    Article  PubMed  CAS  Google Scholar 

  • Dijkerman HC, De Haan EHF (2007) Somatosensory processes subserving perception and action. Behav Brain Sci 30:189–239

    Article  PubMed  Google Scholar 

  • Ehrsson HH, Spence C, Passingham RE (2004) That’s my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305:875–877

    Article  PubMed  CAS  Google Scholar 

  • Elliott D, Chua R, Pollock BJ (1994) The influence of intermittent vision on manual aiming. Acta Psychol 85:1–13

    Article  CAS  Google Scholar 

  • Goble DJ, Brown SH (2008a) The biological and behavioral basis of upper limb asymmetries in sensorimotor performance. Neurosci Biobehav Rev 32:598–610

    Article  PubMed  Google Scholar 

  • Goble DJ, Brown SH (2008b) Upper limb asymmetries in the matching of proprioceptive versus visual targets. J Neurophysiol 99:3063–3074

    Article  PubMed  Google Scholar 

  • Goble DJ, Brown RJ (2009) Dynamic proprioceptive target matching behavior in the upper limb: effects of speed, task difficulty and arm/hemisphere asymmetries. Behav Brain Res 200:7–14

    Article  PubMed  Google Scholar 

  • Gurfinkel VS, Levick YS (1991) Perceptual and automatic aspects of the postural body scheme. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 147–162

    Google Scholar 

  • Hach S, Schütz-Bosbach S (2010) Sinistrals’ upper hand: evidence for handedness differences in the representation of body space. Brain Cognit 72:408–418

    Article  Google Scholar 

  • Halligan PW, Hunt M, Marshall JC, Wade DT (1995) Sensory detection without localization. Neurocase 1:259–266

    Article  Google Scholar 

  • Ishihara M, Imanaka K (2008) Visual perception and motor preparation of manual aiming: a review of behavioral studies and neural correlates. In: Nilsson IL, Lindberg WV (eds) Visual perception: new research. Nova Publishers, Inc, USA, pp 1–48

    Google Scholar 

  • Jewell G, McCourt ME (2000) Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia 38:93–110

    Article  PubMed  CAS  Google Scholar 

  • Kammers MPM, van der Ham IJM, Dijkerman HC (2006) Dissociating body representations in healthy individuals: differential effects of kinaesthetic illusion depending on body representations. Neuropsychologia 44:2430–2436

    Article  PubMed  CAS  Google Scholar 

  • Kammers MPM, De Vignemont F, Verhagen L, Dijkerman HC (2009) The rubber hand illusion in action. Neuropsychologia 47:204–211

    Article  PubMed  CAS  Google Scholar 

  • Kappers AML (2007) Haptic space processing—Allocentric and egocentric reference frames. Can J Exp Psychol 61:208–218

    PubMed  Google Scholar 

  • Ketelaars MAC, Garry MI, Franks IM (1997) On-line programming of simple movement sequences. Human Mov Sci 16:461–483

    Article  Google Scholar 

  • Linkenauger SA, Witt JK, Bakdash JZ, Stefanucci JK, Proffitt DR (2009) Asymmetrical body perception: a possible role for neural body representations. Psychological Science 20:1373–1380

    Article  PubMed  Google Scholar 

  • Longo MR, Haggard P (2010) An implicit body representation underlying human position sense. Proc Nat Acad Sci 107:11727–11732

    Article  PubMed  CAS  Google Scholar 

  • Longo MR, Azanon E, Haggard P (2010) More than skin deep: body representation beyond primary somatosensory cortex. Neuropsychologia 48:655–668

    Article  PubMed  Google Scholar 

  • Marcel AJ (2003) The sense of agency: awareness and ownership of action. In: Roessler J, Eilan N (eds) Agency and self-awareness. Oxford University Press, Oxford

    Google Scholar 

  • Marsh EB, Hillis AE (2008) Dissociation between egocentric and allocentric visuospatial and tactile neglect in acute stroke. Cortex 44:1215–1220

    Article  PubMed  Google Scholar 

  • Milner AD, Goodale MA (1993) Visual pathways to perception and action. Prog Brain Res 95:317–337

    Article  PubMed  CAS  Google Scholar 

  • Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46:774–785

    Article  PubMed  CAS  Google Scholar 

  • Niebauer CL, Aselage J, Schutte C (2002) Hemispheric interaction and consciousness: degree of handedness predicts the intensity of a sensory illusion. Laterality 7:85–96

    PubMed  Google Scholar 

  • Ocklenburg S, Rüther N, Petersburs J, Pinnow M, Güntürkün O (2010) Laterality in the rubber hand illusion. Laterality 16:174–187

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Paillard J (1999) Body schema and body image—a double dissociation in deafferented patients. In: Gantchev GN, Mori S, Massion J (eds) Motor control: today and tomorrow. Academic Publishing House, Sofia, pp 197–214

    Google Scholar 

  • Paillard J (2005) Vectorial versus configural encoding of body space: a neural basis for a distinction between body schema and body image. In: De Preester H, Knockaert V (eds) Body image and body schema: interdisciplanary perspectives on the body. John Benjamins Publishing Company, Amsterdam/Philadelphia, pp 89–110

    Google Scholar 

  • Papula L (1998) Mathematische Formelsammlung fuer Ingeneure und Naturwissenschaftler. Vieweg & Sohn Verlagsgesellschaft mbH, Braunschweig

    Google Scholar 

  • Pozzo T, Stapley PJ, Papaxanthis C (2002) Coordination between equilibrium and hand trajectories during whole body pointing movements. Exp Res 144:343–350

    Article  Google Scholar 

  • Reed CL, Caselli RJ, Farah MJ (1996) Tactile agnosia: underlying impairment and implications for normal tactile object recognition. Brain 119:875–888

    Article  PubMed  Google Scholar 

  • Rossetti Y (1998) Implicit short-lived motor representations of space in brain damaged and healthy subjects. Conscious Cognit 7:520–558

    Article  CAS  Google Scholar 

  • Rossetti Y, Rode G, Boisson D (1995) Implicit processing of somesthetic information: a dissociation between where and how? NeuroReport 6:506–510

    Article  PubMed  CAS  Google Scholar 

  • Rossetti Y, Rode G, Boisson D (2001) Numbsense: a case study and implications. In: de Gelder B, de Haan EHF, Heywood CA (eds) Out of mind: varieties of unconscious processing. Oxford University Press, Oxford, pp 265–292

    Google Scholar 

  • Rossetti Y, Pisella L, Vighetto A (2003) Optic ataxia revisited: visually guided action versus immediate visuomotor control. Exp Brain Res 153:171–179

    Article  PubMed  Google Scholar 

  • Rossetti Y, Revol P, McIntosh RD et al (2005a) Visually guided reaching: bilateral posterior parietal lesions cause a switch from fast visuomotor to slow cognitive control. Neuropsychologia 43:162–177

    Article  PubMed  CAS  Google Scholar 

  • Rossetti Y, Rode G, Farne A, Rossetti A (2005b) Implicit body representations in action. In: De Preester H, Knockaert V (eds) Body image and body schema: interdisciplinary perspectives on the body. John Benjamins Publishing Company, Amsterdam/Philadelphia, pp 111–125

    Google Scholar 

  • Roy EA, Elliott D (1986) Manual asymmetries in visually directed aiming. Can J Psychol 40:109–121

    Article  PubMed  CAS  Google Scholar 

  • Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675

    PubMed  CAS  Google Scholar 

  • Schütz-Bosbach S, Musil JJ, Haggard P (2009) Touchant-Touche: the role of self-touch in the representation of body structure. Conscious Cognit 18:2–11

    Article  Google Scholar 

  • Schwoebel J, Coslett HB (2005) Evidence of multiple, distinct representations of the human body. J Cogn Neurosci 17:543–553

    Article  PubMed  Google Scholar 

  • Steingrueber HJ (1975) Handedness as a function of test complexity. Percept Mot Skills 40:263–266

    PubMed  CAS  Google Scholar 

  • Stoeckel MC, Weder B, Binkofski F et al (2004) Left and right superior parietal lobule in tactile object discrimination. Eur J Neurosci 19:1067–1072

    Article  PubMed  CAS  Google Scholar 

  • Ungerleider MG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, pp 549–586

    Google Scholar 

  • Vallar G, Ronchi R (2009) Somatoparaphrenia: a body delusion. A review of the neuropsychological literature. Exp Brain Res 192:533–551

    Article  PubMed  Google Scholar 

  • Vallar G, Guariglia C, Rusconi ML (1997) Modulation of the neglect syndrome by sensory stimulation. In: Thier P, Karnath H (eds) Parietal lobe contributions to orientation in 3D space. Springer, Berlin, pp 555–578

    Google Scholar 

  • Vogel JL, Bowers CA, Vogel DS (2003) Cerebral lateralisation of spatial abilities: a meta-analysis. Brain Cognit 52:197–204

    Article  Google Scholar 

  • Westwood DA, Goodale MA (2003) Perceptual illusion and the real-time control of action. Spat Vis 16:243–254

    Article  PubMed  Google Scholar 

  • Zuidhoek S, Kappers AML, van der Lubbe RHJ, Postma A (2003) Delay improves performance on a haptic spatial matching task. Exp Brain Res 149:320–330

    PubMed  Google Scholar 

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Acknowledgments

Sylvia Hach and Simone Schütz-Bosbach were supported by a fellowship of Max Planck Society to Simone Schütz-Bosbach. Masami Ishihara was supported by the Max Planck Institute and Deutsche Forschungsgemeinschaft. Peter E. Keller was supported by the Max Planck Society. The authors wish to thank Jan Bergmann for his help with the motion capture system setup and the Matlab scripts for the visualisation of the results.

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  1. Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstr. 1a, 04103, Leipzig, Germany

    Sylvia Hach, Peter E. Keller & Simone Schütz-Bosbach

  2. Tokyo Metropolitan University, Tokyo, Japan

    Masami Ishihara

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  1. Sylvia Hach
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  2. Masami Ishihara
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  4. Simone Schütz-Bosbach
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Correspondence to Sylvia Hach.

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Hach, S., Ishihara, M., Keller, P.E. et al. Hard and fast rules about the body: contributions of the action stream to judging body space. Exp Brain Res 212, 563–574 (2011). https://doi.org/10.1007/s00221-011-2765-1

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