The impact of unilateral brain damage on anticipatory grip force scaling when lifting everyday objects

The scaling of our finger forces according to the properties of manipulated objects is an elementary prerequisite of skilled motor behavior. Lesions of the motor-dominant left brain may impair several aspects of motor planning. For example, limb-apraxia, a tool-use disorder after left brain damage is thought to be caused by deficient recall or integration of tool-use knowledge into an action plan. The aim of the present study was to investigate whether left brain damage affects anticipatory force scaling when lifting everyday objects. We examined 26 stroke patients with unilateral brain damage (16 with left brain damage, ten with right brain damage) and 21 healthy control subjects. Limb apraxia was assessed by testing pantomime of familiar tool-use and imitation of meaningless hand postures. Participants grasped and lifted twelve randomly presented everyday objects. Grip force was measured with help of sensors fixed on thumb, index and middle-finger. The maximum rate of grip force was determined to quantify the precision of anticipation of object properties. Regression analysis yielded clear deficits of anticipation in the group of patients with left brain damage, while the comparison of patient with right brain damage with their respective control group did not reveal comparable deficits. Lesion-analyses indicate that brain structures typically associated with a tool-use network in the left hemisphere play an essential role for anticipatory grip force scaling, especially the left inferior frontal gyrus (IFG) and the premotor cortex (PMC). Furthermore, significant correlations of impaired anticipation with limb apraxia scores suggest shared representations. However, the presence of dissociations, implicates also independent processes. Overall, our findings suggest that the left hemisphere is engaged in anticipatory grip force scaling for lifting everyday objects. The underlying neural substrate is not restricted to a single region or stream; instead it may rely on the intact functioning of a left hemisphere network that may overlap with the left hemisphere dominant tool-use network.

[1]  Melvyn A. Goodale,et al.  Dissociable neural mechanisms for determining the perceived heaviness of objects and the predicted weight of objects during lifting: An fMRI investigation of the size–weight illusion , 2009, NeuroImage.

[2]  D. Kimura,et al.  Left-hemisphere control of oral and brachial movements and their relation to communication. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  Roberto Cubelli,et al.  Double Dissociation between Meaningful and Meaningless Gesture Reproduction in Apraxia , 2001, Cortex.

[4]  R. Johansson,et al.  Experience Can Change Distinct Size-Weight Priors Engaged in Lifting Objects and Judging their Weights , 2008, Current Biology.

[5]  E. Renzi,et al.  Performance of Left Brain-Damaged Patients on Imitation of Single Movements and Motor Sequences. Frontal and Parietal-Injured Patients Compared , 1983, Cortex.

[6]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[7]  Melvyn A. Goodale,et al.  FMRI adaptation during performance of learned arbitrary visuomotor conditional associations , 2009, NeuroImage.

[8]  N. Mai,et al.  A computational procedure for movement analysis in handwriting , 1994, Journal of Neuroscience Methods.

[9]  H. Carnahan,et al.  Unilateral basal ganglia damage causes contralesional force control deficits: A case study , 2005, Neuropsychologia.

[10]  H. Liepmann.  Drei Aufsätze aus dem Apraxiegebiet , 1908 .

[11]  R T Knight,et al.  Spatial deficits in ideomotor limb apraxia. A kinematic analysis of aiming movements. , 1999, Brain : a journal of neurology.

[12]  Simon B. Eickhoff,et al.  On the role of the ventral premotor cortex and anterior intraparietal area for predictive and reactive scaling of grip force , 2008, Brain Research.

[13]  F. Osiurak,et al.  Re-examining the gesture engram hypothesis. New perspectives on apraxia of tool use , 2011, Neuropsychologia.

[14]  S. Frey.  What Puts the How in Where? Tool Use and the Divided Visual Streams Hypothesis , 2007, Cortex.

[15]  N. Motomura,et al.  A Case of Ideational Apraxia with Impairment of Object Use and Preservation of Object Pantomime , 1994, Cortex.

[16]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[17]  Laurel J. Buxbaum,et al.  Deficient internal models for planning hand–object interactions in apraxia , 2005, Neuropsychologia.

[18]  H. Tanabe,et al.  Role of Somatosensory Feedback from Tools in Realizing Movements by Patients with Ideomotor Apraxia , 1999, European Neurology.

[19]  J. Hermsdörfer,et al.  Size–weight illusion and anticipatory grip force scaling following unilateral cortical brain lesion , 2011, Neuropsychologia.

[20]  Gereon R. Fink,et al.  Inhibition of the anterior intraparietal area and the dorsal premotor cortex interfere with arbitrary visuo-motor mapping , 2010, Clinical Neurophysiology.

[21]  Subashan Perera,et al.  Impaired Grip Force Modulation in the Ipsilesional Hand after Unilateral Middle Cerebral Artery Stroke , 2005, Neurorehabilitation and neural repair.

[22]  Yong Li,et al.  Different left brain regions are essential for grasping a tool compared with its subsequent use , 2010, NeuroImage.

[23]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[24]  R. Johansson,et al.  Visual size cues in the programming of manipulative forces during precision grip , 2004, Experimental Brain Research.

[25]  R. Johansson,et al.  Predictive mechanisms and object representations used in object manipulation , 2009 .

[26]  A. Longoni,et al.  Problems in the Assessment of Hand Preference , 1985, Cortex.

[27]  Joachim Hermsdörfer,et al.  Spatial and kinematic features of apraxic movement depend on the mode of execution , 2006, Neuropsychologia.

[28]  Agnès Roby-Brami,et al.  Tool use kinematics across different modes of execution. Implications for action representation and apraxia , 2013, Cortex.

[29]  D. Nowak,et al.  Grip force control during object manipulation in cerebral stroke , 2003, Clinical Neurophysiology.

[30]  J Hermsdörfer,et al.  The effect of tactile feedback on pantomime of tool use in apraxia , 2004, Neurology.

[31]  H. Karnath,et al.  Using human brain lesions to infer function: a relic from a past era in the fMRI age? , 2004, Nature Reviews Neuroscience.

[32]  Susan V. Duff,et al.  The impact of left hemisphere stroke on force control with familiar and novel objects: Neuroanatomic substrates and relationship to apraxia , 2010, Brain Research.

[33]  G. Goldenberg,et al.  Hemisphere asymmetries for imitation of novel gestures , 2002, Neurology.

[34]  D. Nowak,et al.  Dexterity in cerebellar agenesis , 2007, Neuropsychologia.

[35]  Georg Goldenberg,et al.  Defective pantomime of object use in left brain damage: apraxia or asymbolia? , 2003, Neuropsychologia.

[36]  N. Geschwind.  The apraxias: neural mechanisms of disorders of learned movement. , 1975, American scientist.

[37]  K. Heilman,et al.  Cortical and subcortical contributions to ideomotor apraxia: analysis of task demands and error types. , 2001, Brain : a journal of neurology.

[38]  A. Meltzoff,et al.  An fMRI study of imitation: action representation and body schema , 2005, Neuropsychologia.

[39]  J. Flanagan,et al.  Independence of perceptual and sensorimotor predictions in the size–weight illusion , 2000, Nature Neuroscience.

[40]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[41]  A. G. Witney,et al.  Learning and decay of prediction in object manipulation. , 2000, Journal of neurophysiology.

[42]  Alan Sunderland,et al.  Tool use and action planning in apraxia , 2011, Neuropsychologia.

[43]  Robert L. Sainburg,et al.  Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy , 2009, Neuropsychologia.

[44]  K. J. Cole.  Lifting a familiar object: visual size analysis, not memory for object weight, scales lift force , 2008, Experimental Brain Research.

[45]  Marco Davare,et al.  Causal Connectivity between the Human Anterior Intraparietal Area and Premotor Cortex during Grasp , 2010, Current Biology.

[46]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[47]  Georg Goldenberg,et al.  The Neural Basis of Imitation is Body Part Specific , 2006, The Journal of Neuroscience.

[48]  Gereon R Fink,et al.  Dexterity is impaired at both hands following unilateral subcortical middle cerebral artery stroke , 2007, The European journal of neuroscience.

[49]  Will Spijkers,et al.  From pantomime to actual use: How affordances can facilitate actual tool-use , 2011, Neuropsychologia.

[50]  I Salimi,et al.  Specificity of internal representations underlying grasping. , 2000, Journal of neurophysiology.

[51]  Joachim Hermsdörfer,et al.  Anticipatory scaling of grip forces when lifting objects of everyday life , 2011, Experimental Brain Research.

[52]  K. J. Cole,et al.  Memory representations underlying motor commands used during manipulation of common and novel objects. , 1993, Journal of neurophysiology.

[53]  P Jenmalm,et al.  Visual and Somatosensory Information about Object Shape Control Manipulative Fingertip Forces , 1997, The Journal of Neuroscience.

[54]  Kenneth M. Heilman,et al.  Apraxia : The Neuropsychology of Action , 2014 .

[55]  G. Goldenberg,et al.  Severity of neglect predicts accuracy of imitation in patients with right hemisphere lesions , 2009, Neuropsychologia.

[56]  R. Johansson,et al.  Sensorimotor prediction and memory in object manipulation. , 2001, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[57]  A. Gordon,et al.  Fingertip forces during object manipulation in children with hemiplegic cerebral palsy. I: Anticipatory scaling , 1999, Developmental medicine and child neurology.

[58]  K. J. Cole,et al.  Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp , 2002, Experimental Brain Research.

[59]  K. Amunts,et al.  Broca's region subserves imagery of motion: A combined cytoarchitectonic and fMRI study , 2000, Human brain mapping.

[60]  J Hermsdörfer,et al.  Size-weight illusion, anticipation, and adaptation of fingertip forces in patients with cerebellar degeneration. , 2009, Journal of neurophysiology.

[61]  K. Heilman,et al.  The Significance of Body Part as Tool Errors in Limb Apraxia , 1997, Brain and Cognition.

[62]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[63]  Alessia Tessari,et al.  Neuropsychological evidence for a strategic control of multiple routes in imitation. , 2006, Brain : a journal of neurology.

[64]  H. Forssberg,et al.  Coordination of Manipulative Forces in Parkinson's Disease , 1997, Experimental Neurology.

[65]  G. R. Fink,et al.  Arbitrary visuomotor mapping in the grip-lift task: dissociation of performance deficits in right and left middle cerebral artery stroke , 2012, Neuroscience.

[66]  J. Hermsdörfer,et al.  Grip forces isolated from knowledge about object properties following a left parietal lesion , 2007, Neuroscience Letters.

[67]  Robert L Sainburg,et al.  Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. , 2007, Brain : a journal of neurology.

[68]  Steven Laureys,et al.  Imaging a cognitive model of apraxia: The neural substrate of gesture‐specific cognitive processes , 2004, Human brain mapping.

[69]  A. M. Smith,et al.  Friction, not texture, dictates grip forces used during object manipulation. , 1996, Journal of neurophysiology.

[70]  Andrew M Gordon,et al.  Learning of grasp control in children with hemiplegic cerebral palsy. , 2003, Developmental medicine and child neurology.

[71]  Leif Johannsen,et al.  Tool use without a tool: kinematic characteristics of pantomiming as compared to actual use and the effect of brain damage , 2012, Experimental Brain Research.

[72]  G. Goldenberg,et al.  The meaning of meaningless gestures: A study of visuo-imitative apraxia , 1997, Neuropsychologia.

[73]  Chris Rorden,et al.  Pantomime of tool use depends on integrity of left inferior frontal cortex. , 2007, Cerebral cortex.

[74]  Angela Sirigu,et al.  A Selective Impairment of Hand Posture for Object Utilization in Apraxia , 1995, Cortex.

[75]  L. Buxbaum.  Ideomotor Apraxia: a Call to Action , 2001, Neurocase.

[76]  K M Heilman,et al.  Spatial planning deficits in limb apraxia. , 1994, Brain : a journal of neurology.

[77]  Joachim Hermsdörfer,et al.  Object properties and cognitive load in the formation of associative memory during precision lifting , 2009, Behavioural Brain Research.

[78]  Murray Grossman,et al.  Left Inferior Parietal Representations for Skilled Hand-Object Interactions: Evidence from Stroke and Corticobasal Degeneration , 2007, Cortex.

[79]  R. Johansson,et al.  Integration of sensory information during the programming of precision grip: comments on the contributions of size cues , 2004, Experimental Brain Research.

[80]  G. Goldenberg.  Apraxia and the parietal lobes , 2009, Neuropsychologia.

[81]  M. Jeannerod,et al.  The timing of mentally represented actions , 1989, Behavioural Brain Research.

[82]  L. Buxbaum,et al.  The Role of the Dynamic Body Schema in Praxis: Evidence from Primary Progressive Apraxia , 2000, Brain and Cognition.

[83]  K. Heilman,et al.  Two forms of ideomotor apraxia , 1982, Neurology.