Top

Published in:

01-10-2011 | Research Article

Preserved grip selection planning in chronic unilateral upper extremity amputees

Authors: Benjamin A. Philip, Scott H. Frey

Published in: Experimental Brain Research | Issue 3/2011

Abstract

Upper limb amputees receive no proprioceptive or visual sensory feedback about their absent hand. In this study, we asked whether chronic amputees nevertheless retain the ability to accurately plan gripping movements. Fourteen patients and matched controls performed two grip selection tasks: overt grip selection (OGS), in which they used their intact hand to grasp an object that appeared in different orientations using the most natural (under- or overhand) precision grip, and prospective grip selection (PGS), in which they selected the most natural grip for either hand without moving. We evaluated planning accuracy by comparing concordance between grip preferences expressed in PGS vs. OGS for the intact hand and PGS vs. the inverse of OGS responses for the affected hand. Overall, amputees showed no deficits in the accuracy of grip selection planning based on either hand and a consistent preference for less awkward hand postures. We found no evidence for a speed-accuracy tradeoff. Furthermore, selection accuracy did not depend on phantom mobility, phantom limb pain, time since amputation, or the residual limb’s shoulder posture. Our findings demonstrate that unilateral upper limb amputees retain the ability to plan movements based on the biomechanics of their affected hand even many years after limb loss. This unimpaired representation may stem from persistent higher-level activity-independent internal representations or may be sustained by sensory feedback from the intact hand.

Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285(5425):257–260PubMedCrossRef

Buneo CA, Andersen RA (2006) The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44(13):2594–2606. doi:10.1016/j.neuropsychologia.2005.10.011 PubMedCrossRef

Daprati E, Nico D, Duval S, Lacquaniti F (2010) Different motor imagery modes following brain damage. Cortex 46(8):1016–1030. doi:10.1016/j.cortex.2009.08.002 PubMedCrossRef

Datta D, Selvarajah K, Davey N (2004) Functional outcome of patients with proximal upper limb deficiency—acquired and congenital. Clin rehabil 18(2):172–177PubMedCrossRef

de Lange FP, Helmich RC, Toni I (2006) Posture influences motor imagery: an fMRI study. NeuroImage 33(2):609–617. doi:10.1016/j.neuroimage.2006.07.017 PubMedCrossRef

Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2(6):563–567. doi:10.1038/9219 PubMedCrossRef

Donoghue JP, Sanes JN (1988) Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats. J Neurosci 8(9):3221–3232PubMed

Frey SH (2010) Forecasting the long-range consequences of manual and tool use actions: neurophysiological, behavioral and computational considerations. In: Danion F, Latash ML (eds) Motor control: theories, experiments and applications. Oxford University Press, New York, pp 295–313

Grush R (2004) The emulation theory of representation: motor control, imagery, and perception. Behav Brain Sci 27(3):377–396 (discussion 396–442)PubMed

Haber WB (1958) Reactions to loss of limb: physiological and psychological aspects. Ann NY Acad Sci 74(1):14–24

Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, Branner A, Chen D, Penn RD, Donoghue JP (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442(7099):164–171. doi:10.1038/nature04970 PubMedCrossRef

Ionta S, Blanke O (2009) Differential influence of hands posture on mental rotation of hands and feet in left and right handers. Exp Brain Res 195(2):207–217. doi:10.1007/s00221-009-1770-0 PubMedCrossRef

Jacobs S, Danielmeier C, Frey SH (2010) Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool. J Cogn Neurosci 22(11):2594–2608. doi:10.1162/jocn.2009.21372 PubMedCrossRef

James MA, Bagley AM, Brasington K, Lutz C, McConnell S, Molitor F (2006) Impact of prostheses on function and quality of life for children with unilateral congenital below-the-elbow deficiency. J Bone Jount Surg Am 88(11):2356–2365. doi:10.2106/JBJS.E.01146 CrossRef

Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17(2):187–245

Jenkinson PM, Edelstyn NMJ, Ellis SJ (2009) Imagining the impossible: motor representations in anosognosia for hemiplegia. Neuropsychologia 47(2):481–488. doi:10.1016/j.neuropsychologia.2008.10.004 PubMedCrossRef

Johnson SH (1998) Cerebral organization of motor imagery: contralateral control of grip selection in mentally represented prehension. Psychol Sci 9:219–222CrossRef

Johnson SH (2000a) Thinking ahead: the case for motor imagery in prospective judgements of prehension. Cognition 74(1):33–70PubMedCrossRef

Johnson SH (2000b) Imagining the impossible: intact motor representations in hemiplegics. NeuroReport 11(4):729–732PubMedCrossRef

Johnson SH, Sprehn G, Saykin AJ (2002a) Intact motor imagery in chronic upper limb hemiplegics: evidence for activity-independent action representations. J Cogn Neurosci 14(6):841–852. doi:10.1162/089892902760191072 PubMedCrossRef

Johnson SH, Rotte M, Grafton ST, Hinrichs H, Gazzaniga MS, Henize J-H (2002b) Selective activation of a parietofrontal circuit during implicitly imagined prehension. NeuroImage 17(4):1693–1704PubMedCrossRef

Kaas JH (2000) The reorganization of somatosensory and motor cortex after peripheral nerve or spinal cord injury in primates. Prog Brain Res 128:173–179PubMedCrossRef

Kawashima R, Roland PE, O’Sullivan BT (1994) Activity in the human primary motor cortex related to ipsilateral hand movements. Brain Res 663(2):251–256PubMedCrossRef

Koeneke S, Lutz K, Herwig U, Ziemann U, Jäncke L (2006) Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp Brain Res 174(2):199–209. doi:10.1007/s00221-006-0440-8 PubMedCrossRef

Lee M, Hinder MR, Gandevia SC, Carroll TJ (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588(1):201–212. doi:10.1113/jphysiol.2009.183855 PubMedCrossRef

Lotze M, Grodd W, Birbaumer N, Erb M, Huse E, Flor H (1999) Does use of a myoelectric prosthesis prevent cortical reorganization and phantom limb pain? Nat Neurosci 2(6):501–502PubMedCrossRef

MacKenzie CL, Iberall T (1994) The grasping hand. Elsevier, Amsterdam

Marangon M, Jacobs S, Frey SH (in press) Context-sensitivity of grasp representations in human rostral inferior parietal lobule. J Neurophysiol

Mercier C, Reilly KT, Vargas CD, Aballea A, Sirigu A (2006) Mapping phantom movement representations in the motor cortex of amputees. Brain 129(8):2202–2210. doi:10.1093/brain/awl180 PubMedCrossRef

Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D (1983) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8(1):33–55PubMedCrossRef

Moore CJ, Price CJ (1999) A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain 122(5):943–962PubMedCrossRef

Moore CE, Schady W (2000) Investigation of the functional correlates of reorganization within the human somatosensory cortex. Brain 123(9):1883–1895PubMedCrossRef

Nico D, Daprati E, Rigal F, Parsons L, Sirigu A (2004) Left and right hand recognition in upper limb amputees. Brain 127(1):120–132. doi:10.1093/brain/awh006 PubMedCrossRef

Parlow SE, Kinsbourne M (1989) Asymmetrical transfer of training between hands: implications for interhemispheric communication in normal brain. Brain Cogn 11(1):98–113PubMedCrossRef

Parsons LM (1994) Temporal and kinematic properties of motor behavior reflected in mentally simulated action. J Exp Psychol Hum Percept Perform 20(4):709–730PubMedCrossRef

Pascual-Leone A, Peris M, Tormos JM, Pascual AP, Catalá MD (1996) Reorganization of human cortical motor output maps following traumatic forearm amputation. NeuroReport 7(13):2068–2070PubMedCrossRef

Perez MA, Tanaka S, Wise SP, Sadato N, Tanabe HC, Willingham DT, Cohen LG (2007a) Neural substrates of intermanual transfer of a newly acquired motor skill. Curr Biol 17(21):1896–1902. doi:10.1016/j.cub.2007.09.058 PubMedCrossRef

Perez M, Wise S, Willingham D, Cohen L (2007b) Neurophysiological mechanisms involved in transfer of procedural knowledge. J Neurosci 27(5):1045–1053PubMedCrossRef

Philip BA, Frey SH (2010) Intact prediction of grip selection with an amputated hand. Program No. 291.13. 2010 Neuroscience Meeting Planner. Society for Neuroscience, San Diego, CA (Online)

Raffin E, Giraux P, Reilly KT (2011) The moving phantom: motor execution or motor imagery? Cortex. (epub ahead of print). doi:10.1016/j.cortex.2011.02.003

Sanes JN, Suner S, Lando JF, Donoghue JP (1988) Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. Proc Natl Acad Sci USA 85(6):2003–2007PubMedCrossRef

Shadmehr R, Krakauer J (2008) A computational neuroanatomy for motor control. Exp Brain Res 185(3):359–381. doi:10.1007/s00221-008-1280-5 PubMedCrossRef

Shenton JT, Schwoebel J, Branch HB (2004) Mental motor imagery and the body schema: evidence for proprioceptive dominance. Neurosci Lett 370(1):19–24. doi:10.1016/j.neulet.2004.07.053 PubMedCrossRef

Sirigu A, Duhamel JR (2001) Motor and visual imagery as two complementary but neurally dissociable mental processes. J Cogn Neurosci 13(7):910–919

Tomasino B, Rumiati RI (2004) Effects of strategies on mental rotation and hemispheric lateralization: neuropsychological evidence. J Cogn Neurosci 16(5):878–888. doi:10.1162/089892904970753 PubMedCrossRef

Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11(18):R729–R732PubMedCrossRef

Wolpert D, Miall R (1996) Forward models for physiological motor control. Neural Netw 9(8):1265–1279. doi:papers://9ECEC99B-FEEC-4808-A2E1-EB1DC6D0033D/Paper/p503 PubMedCrossRef

Wolpert DM, Goodbody SJ, Husain M (1998) Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci 1(6):529–533. doi:10.1038/2245 PubMedCrossRef

Wright TW, Hagen AD, Wood MB (1995) Prosthetic usage in major upper extremity amputations. J Hand Surg Am 20(4):619–622. doi:10.1016/S0363-5023(05)80278-3 PubMedCrossRef

Title: Preserved grip selection planning in chronic unilateral upper extremity amputees
Authors: Benjamin A. Philip
Scott H. Frey
Publication date: 01-10-2011
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 3/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-011-2842-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Preserved grip selection planning in chronic unilateral upper extremity amputees

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2011

Anticipation of future events improves the ability to estimate elapsed time

Comment on: Exp Brain Res. 2011 May 5th. Transcranial magnetic stimulation of macaque frontal eye fields decreases saccadic reaction time. Gerits A, Ruff CC, Guipponi O, Wenderoth N, Driver J, Vanduffel W

Fast and fine-tuned corrections when the target of a hand movement is displaced

Potentiation of spontaneous and evoked cortical electrical activity after spreading depression: in vivo analysis in well-nourished and malnourished rats

Visual signals bias auditory targets in azimuth and depth

Timing movements to interval durations specified by discrete or continuous sounds