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Tool use without a tool: kinematic characteristics of pantomiming as compared to actual use and the effect of brain damage

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Abstract

Movement goals and task mechanics differ substantially between actual tool use and corresponding pantomimes. In addition, apraxia seems to be more severe during pantomime than during actual tool use. Comparisons of these two modes of action execution using quantitative methods of movement analyses are rare. In the present study, repetitive scooping movements with a ladle from a bowl into a plate were recorded and movement kinematics was analyzed. Brain-damaged patients using their ipsilesional hand and healthy control subjects were tested in three conditions: pantomime, demonstration with the tool only, and actual use in the normal context. Analysis of the hand trajectories during the transport component revealed clear differences between the tasks, such as slower actual use and moderate deficits in patients with left brain damage (LBD). LBD patients were particularly impaired in the scooping component: LBD patients with apraxia exhibited reduced hand rotation at the bowl and the plate. The deficit was most obvious during pantomime but actual use was also affected, and reduced hand rotation was consistent across conditions as indicated by strong pair-wise correlations between task conditions. In healthy control subjects, correlations between movement parameters were most evident between the pantomime and demonstration conditions but weak in correlation pairs involving actual use. From these findings and published neuroimaging evidence, we conclude that for a specific tool-use action, common motor schemas are activated but are adjusted and modified according to the actual task constraints and demands. An apraxic LBD individual can show a deficit across all three action conditions, but the severity can differ substantially between conditions.

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References

  • Buxbaum LJ, Giovannetti T, Libon D (2000) The role of the dynamic body schema in praxis: evidence from primary progressive apraxia. Brain Cogn 44:166–191

    Article  PubMed  CAS  Google Scholar 

  • Clark MA, Merians AS, Kothari A, Poizner H, Macauley B, Rothi LJG, Heilman KM (1994) Spatial planning deficits in limb apraxia. Brain 117:1093–1106

    Article  PubMed  Google Scholar 

  • Daprati E, Sirigu A (2006) How we interact with objects: learning from brain lesions. Trends Cogn Sci 10:265–270

    Article  PubMed  Google Scholar 

  • De Renzi E (1990) Apraxia. In: Boller F, Grafman J (eds) Handbook of clinical neuropsychology, vol 2. Elsevier, Amsterdam, New York, pp 245–263

    Google Scholar 

  • De Renzi E, Luchelli F (1988) Ideational apraxia. Brain 111:1173–1185

    Article  PubMed  Google Scholar 

  • De Renzi E, Faglioni P, Sorgato P (1982) Modality-specific and supramodal mechanisms of apraxia. Brain 105:301–312

    Article  PubMed  Google Scholar 

  • Filimon F, Nelson JD, Hagler DJ, Sereno MI (2007) Human cortical representations for reaching: mirror neurons for execution, observation, and imagery. Neuroimage 37:1315–1328

    Article  PubMed  Google Scholar 

  • Fisk JD, Goodale MA (1988) The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit. Exp Brain Res 72:425–435

    Article  PubMed  CAS  Google Scholar 

  • Gerardin E, Sirigu A, Lehéricy S, Poline J-B, Gaymard B, Marsault C, Agid Y, Le Bihan D (2000) Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex 10:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg G (1996) Defective imitation of gestures in patients with damage in the left or right hemispheres. J Neurol Neurosurg Psychiatry 61:176–180

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg G (2008) Apraxia. In: Goldenberg G, Miller B (eds) Handbook of clinical neurology—neuropsychology and behavior. Elsevier, Edinburgh, pp 323–338

  • Goldenberg G, Hagmann S (1998) Tool use and mechanical problem solving in apraxia. Neuropsychologia 36:581–589

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg G, Spatt J (2009) The neural basis of tool use. Brain 132:1645–1655

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg G, Hartmann K, Schlott I (2003) Defective pantomime of object use in left brain damage: apraxia or asymbolia? Neuropsychologia 41:1565–1573

    Article  PubMed  Google Scholar 

  • Goldenberg G, Hentze S, Hermsdörfer J (2004) The effect of tactile feedback on pantomime of tool use in apraxia. Neurology 63:1863–1867

    PubMed  CAS  Google Scholar 

  • Goodale MA, Jakobson LS, Keillor JM (1994) Differences in the visual control of pantomimed and natural grasping movements. Neuropsychologia 32:1159–1178

    Article  PubMed  CAS  Google Scholar 

  • Grèzes J, Decety J (2001) Functional anatomy of execution, mental simulation, observation, and verb generation of actions: a meta-analysis. Hum Brain Map 12:1–19

    Article  Google Scholar 

  • Haaland KY, Harrington DL (1994) Limb-sequencing deficits after left but not right hemisphere damage. Brain Cogn 24:104–122

    Article  PubMed  CAS  Google Scholar 

  • Haaland KY, Prestopnik JL, Knight RT, Lee RR (2004) Hemispheric asymmetries for kinematic and positional aspects of reaching. Brain 127:1145–1158

    Article  PubMed  Google Scholar 

  • Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 18:2775–2788

    Article  PubMed  Google Scholar 

  • Hanna-Pladdy B, Heilman KM, Foundas AL (2001) Cortical and subcortical contributions to ideomotor apraxia: analysis of task demands and error types. Brain 124:2513–2527

    Article  PubMed  CAS  Google Scholar 

  • Hermsdörfer J, Goldenberg G (2002) Ipsilesional deficits during fast diadocokinetic hand movements following unilateral brain damage. Neuropsychologia 40:2100–2115

    Article  PubMed  Google Scholar 

  • Hermsdörfer J, Blankenfeld H, Goldenberg G (2003) The dependence of ipsilesional aiming deficits on task demands, lesioned hemisphere, and apraxia. Neuropsychologia 41:1628–1643

    Article  PubMed  Google Scholar 

  • Hermsdörfer J, Hentze S, Goldenberg G (2006) Spatial and kinematic features of apraxic movement depend on the mode of execution. Neuropsychologia 44:1642–1652

    Article  PubMed  Google Scholar 

  • Hermsdörfer J, Terlinden G, Mühlau M, Goldenberg G, Wohlschläger AM (2007) Neural representations of pantomimed and actual tool use: evidence from an event-related fMRI study. NeuroImage 36:109–118

    Article  Google Scholar 

  • Hermsdörfer J, Li Y, Randerath J, Roby-Brami A, Goldenberg G (2011) Tool use kinematics across different modes of execution. Implications for movement planning and apraxia. Cortex (in press)

  • Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14:S103–S109

    Article  PubMed  CAS  Google Scholar 

  • Johnson-Frey SH (2004) The neural bases of complex tool use in humans. Trends Cogn Sci 8:71–78

    Article  PubMed  Google Scholar 

  • Laimgruber K, Goldenberg G, Hermsdörfer J (2005) Manual and hemispheric asymmetries in the execution of actual and pantomimed prehension. Neuropsychologia 43:682–692

    Article  PubMed  Google Scholar 

  • Lewis JW (2006) Cortical networks related to human use of tools. Neuroscientist 12:211–231

    Article  PubMed  Google Scholar 

  • Liepmann H (1908) Drei Aufsätze aus dem Apraxiegebiet. Karger, Berlin

    Google Scholar 

  • Lotze M, Montoya P, Erb M, Hulsmann E, Flor H, Klose U, Birbaumer N, Grodd W (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements—an Fmri study. J Cogn Neurosci 11:491–501

    Article  PubMed  CAS  Google Scholar 

  • Osiurak F, Jarry C, Allain P, Aubin G, Etcharry-Bouyx F, Richard I, Bernard I, Le GD (2009) Unusual use of objects after unilateral brain damage. The technical reasoning model. Cortex 45:769–783

    Article  PubMed  Google Scholar 

  • Osiurak F, Jarry C, Le Gall D (2011) Re-examining the gesture engram hypothesis. New perspectives on apraxia of tool use. Neuropsychologia (in press, corrected proof)

  • Poizner H, Clark MA, Merians AS, Macauley B, Rothi LJG, Heilman KM (1995) Joint coordination deficits in limb apraxia. Brain 118:227–242

    Article  PubMed  Google Scholar 

  • Randerath J, Li Y, Goldenberg G, Hermsdörfer J (2009) Grasping tools: effects of task and apraxia. Neuropsychologia 47:497–505

    Article  PubMed  Google Scholar 

  • Randerath J, Goldenberg G, Spijkers W, Li Y, Hermsdörfer J (2010) Different left brain regions are essential for grasping a tool compared with its subsequent use. NeuroImage 53:171–180

    Article  PubMed  Google Scholar 

  • Randerath J, Spijkers W, Goldenberg G, Li Y, Hermsdörfer J (2011) From Pantomime to actual use: how affordances can facilitate actual tool-use. Neuropsychologia 49:2410–2416

    Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149–154

    Article  PubMed  CAS  Google Scholar 

  • Rothi LJG, Heilman KM (1997) Apraxia: the neuropsychology of action. Psychology Press, East Sussex

    Google Scholar 

  • Rothi LJG, Raymer AM, Heilman KM (1997) Limb praxis assessment. In: Rothi LJG, Heilman KM (eds) Apraxia: the neuropsychology of action. Psychology Press, East Sussex, pp 61–73

    Google Scholar 

  • Roy EA, Black SE, Barbour K, Mcguiness K, Kalbfleisch L (1998) Pantomime and imitation of hand gestures following stroke. Brain Cogn 37:127–129

    Google Scholar 

  • Salmaso D, Longoni AM (1985) Problems in the assessment of hand preference. Cortex 21:533–549

    PubMed  CAS  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 

  • Schaefer SY, Haaland KY, Sainburg RL (2009) Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy. Neuropsychologia 47:2953–2966

    Article  PubMed  Google Scholar 

  • Schmidt RA (1975) A schema theory of discrete motor skill learning. Psychol Rev 82:225–260

    Article  Google Scholar 

  • Sirigu A, Cohen L, Duhamel JR, Pillon B, Dubois B, Agid Y (1995) A selective impairment of hand posture for object utilization in apraxia. Cortex 31:41–55

    PubMed  CAS  Google Scholar 

  • Wada Y, Nakagawa Y, Nishikawa T, Aso N, Inokawa M, Kashiwagi A, Tanabe H, Takeda M (1999) Role of somatosensory feedback from tools in realizing movements by patients with ideomotor apraxia. Eur Neurol 41:73–78

    Article  PubMed  CAS  Google Scholar 

  • Westwood DA, Schweizer TA, Heath MD, Roy EA, Dixon MJ, Black SE (2001) Transitive gesture production in apraxia: visual and nonvisual sensory contributions. Brain Cogn 46:300–304

    Article  PubMed  CAS  Google Scholar 

  • Winstein CJ, Pohl PS (1995) Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res 105:163–174

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was supported by the grants from the German Federal Ministry of Education and Research (BMBF, project 01GW0572), the German research foundation (DFG, project HE 3592/7-1) and by the FP7 CogWatch project (EC grant 288912).

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Correspondence to Joachim Hermsdörfer.

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Hermsdörfer, J., Li, Y., Randerath, J. et al. Tool use without a tool: kinematic characteristics of pantomiming as compared to actual use and the effect of brain damage. Exp Brain Res 218, 201–214 (2012). https://doi.org/10.1007/s00221-012-3021-z

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  • DOI: https://doi.org/10.1007/s00221-012-3021-z

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