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Rethinking the Cognitive Mechanisms Underlying Pantomime of Tool Use: Evidence from Alzheimer’s Disease and Semantic Dementia

Published online by Cambridge University Press:  16 February 2017

Mathieu Lesourd ,
Josselin Baumard ,
Christophe Jarry ,
Frédérique Etcharry-Bouyx ,
Serge Belliard ,
Olivier Moreaud ,
Bernard Croisile ,
Valérie Chauviré ,
Marine Granjon  and
Didier Le Gall
...Show all authors
Mathieu Lesourd*
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France Service de Neuropsychologie, Hôpital Neurologique Pierre Wertheimer, Bron, France
Josselin Baumard
Affiliation:
Laboratoire de Psychologie des Pays de la Loire (EA4638), Université d’Angers, France Unité de Neuropsychologie, Département de Neurologie, Centre Hospitalier Universitaire d’Angers, France
Christophe Jarry
Affiliation:
Laboratoire de Psychologie des Pays de la Loire (EA4638), Université d’Angers, France Unité de Neuropsychologie, Département de Neurologie, Centre Hospitalier Universitaire d’Angers, France
Frédérique Etcharry-Bouyx
Affiliation:
Laboratoire de Psychologie des Pays de la Loire (EA4638), Université d’Angers, France Unité de Neuropsychologie, Département de Neurologie, Centre Hospitalier Universitaire d’Angers, France
Serge Belliard
Affiliation:
Service de Neurologie, Centre Hospitalier Universitaire, Rennes, France Laboratoire de Neuropsychologie, Unité INSERM U 1077, Caen, France
Olivier Moreaud
Affiliation:
CMRR Grenoble Arc Alpin, Pôle de Psychiatrie et Neurologie, Centre Hospitalier Universitaire de Grenoble, France Laboratoire de Psychologie et Neurocognition CNRS UMR 5105, Grenoble, France
Bernard Croisile
Affiliation:
Service de Neuropsychologie, Hôpital Neurologique Pierre Wertheimer, Bron, France
Valérie Chauviré
Affiliation:
Département de Neurologie, Centre Hospitalier Universitaire d’Angers, France
Marine Granjon
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France
Didier Le Gall
Affiliation:
Laboratoire de Psychologie des Pays de la Loire (EA4638), Université d’Angers, France Unité de Neuropsychologie, Département de Neurologie, Centre Hospitalier Universitaire d’Angers, France
François Osiurak
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France InstitutUniversitaire de France, Paris, France
*
Correspondence and reprint requests to: Mathieu Lesourd, Laboratoired’Etude des MécanismesCognitifs (EA 3082), Institut de Psychologie, 5, avenue Pierre Mendès-France, 69676 BronCedex, France. E-mail: [email protected]
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Abstract

Objectives: Pantomiming the use of familiar tools is a central test in the assessment of apraxia. However, surprisingly, the nature of the underlying cognitive mechanisms remains an unresolved issue. The aim of this study is to shed a new light on this issue by exploring the role of functional, mechanical, and manipulation knowledge in patients with Alzheimer’s disease and semantic dementia and apraxia of tool use. Methods: We performed multiple regression analyses with the global performance and the nature of errors (i.e., production and conception) made during a pantomime of tool use task in patients and control participants as dependent variables and tasks investigating functional, mechanical, and manipulation knowledge as predictors. Results: We found that mechanical problem solving, assessing mechanical knowledge, was a good predictor of the global performance of pantomime of tool use. We also found that occurrence of conception errors was robustly predicted by the task assessing functional knowledge whereas that of production errors was not explained by only one predictor. Conclusions: Our results suggest that both functional and mechanical knowledge are important to pantomime the use of tools. To our knowledge, this is the first demonstration that mechanical knowledge plays a role in pantomime of tool use. Although impairment in pantomime of tool use tasks (i.e., apraxia) is widely explained by the disruption of manipulation knowledge, we propose that pantomime of tool use is a complex problem-solving task. (JINS, 2017, 23, 128–138)

Keywords

ApraxiaAlzheimer’s diseaseSemantic dementiaManipulation knowledgeMechanical knowledgeFunctional knowledgePantomime of tool use
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Special Issue 2: Special Issue: Motor Cognition , February 2017 , pp. 128 - 138
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

Adlam, A.R., Bozeat, S., Arnold, R., Watson, P., & Hodges, J.R. (2006). Semantic knowledge in mild cognitive impairment and mild Alzheimer’s disease. Cortex, 42(5), 675–684. http://doi.org/10.1016/S0010-9452(08)70404-0 Google Scholar
Agresti, A. (2007). An introduction to categorical analysis. Hoboken: Wiley.Google Scholar
Bartolo, A., & Cubelli, R. (2014). The cognitive models of limb apraxia and the specific properties of meaningful gestures. Cortex, 57, 297–298. http://doi.org/10.1016/j.cortex.2014.01.007 CrossRefGoogle ScholarPubMed
Bartolo, A., Cubelli, R., Della Sala, S., & Drei, S. (2003). Pantomimes are special gestures which rely on working memory. Brain and Cognition, 53(3), 483–494. http://doi.org/10.1016/S0278-2626(03)00209-4 Google Scholar
Buxbaum, L.J. (2001). Ideomotor apraxia: A call to action. Neurocase, 7, 445–448.CrossRefGoogle ScholarPubMed
Buxbaum, L.J., Kyle, K., Grossman, M., & Coslett, H.B. (2007). Left inferior parietal representations for skilled hand-object interactions: Evidence from stroke and corticobasal degeneration. Cortex, 43(3), 411–423. http://doi.org/10.1016/S0010-9452(08)70466-0 Google Scholar
Buxbaum, L.J., Kyle, K.M., & Menon, R. (2005). On beyond mirror neurons: Internal representations subserving imitation and recognition of skilled object-related actions in humans. Cognitive Brain Research, 25(1), 226–239. http://doi.org/10.1016/j.cogbrainres.2005.05.014 Google Scholar
Buxbaum, L.J., & Saffran, E.M. (2002). Knowledge of object manipulation and object function: Dissociations in apraxic and nonapraxic subjects. Brain and Language, 82(2), 179–199. http://doi.org/10.1016/S0093-934X(02)00014-7 CrossRefGoogle ScholarPubMed
Buxbaum, L.J., Sirigu, A., Schwartz, M.F., & Klatzky, R. (2003). Cognitive representations of hand posture in ideomotor apraxia. Neuropsychologia, 41(8), 1091–1113. http://doi.org/10.1016/S0028-3932(02)00314-7 CrossRefGoogle ScholarPubMed
Corbett, F., Jefferies, E., Burns, A., & Lambon Ralph, M.A. (2015). Deregulated semantic cognition contributes to object-use deficits in Alzheimer’s disease: A comparison with semantic aphasia and semantic dementia. Journal of Neuropsychology, 9, 219–241. http://doi.org/10.1111/jnp.12047 Google Scholar
Derouesné, C., Lagha-Pierucci, S., Thibault, S., Baudouin-Madec, V., & Lacomblez, L. (2000). Apraxic disturbances in patients with mild to moderate Alzheimer’s disease. Neuropsychologia, 38(13), 1760–1769. http://doi.org/10.1016/S0028-3932(00)00081-6 Google Scholar
Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2000). The FAB: A frontal assessment battery at bedside. Neurology, 55(11), 1621–1626. http://doi.org/10.1212/WNL.57.3.565 CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198. http://doi.org/10.1016/0022-3956(75)90026-6 Google Scholar
Goldenberg, G. (2013). Apraxia: The cognitive side of motor control. Oxford: Oxford University Press, http://doi.org/10.1093/acprof:oso/9780199591510.001.0001 Google Scholar
Goldenberg, G., & Hagmann, S. (1998). Tool use and mechanical problem solving in apraxia. Neuropsychologia, 36(7), 581–589. http://doi.org/S0028-3932(97)00165-6 [pii] Google Scholar
Goldenberg, G., Hartmann, K., & Schlott, I. (2003). Defective pantomime of object use in left brain damage: Apraxia or asymbolia? Neuropsychologia, 41(12), 1565–1573. http://doi.org/10.1016/S0028-3932(03)00120-9 Google Scholar
Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(6), 1645–1655. http://doi.org/10.1093/brain/awp080 Google Scholar
Hartmann, K., Goldenberg, G., Daumüller, M., & Hermsdörfer, J. (2005). It takes the whole brain to make a cup of coffee: The neuropsychology of naturalistic actions involving technical devices. Neuropsychologia, 43(4), 625–637. http://doi.org/10.1016/j.neuropsychologia.2004.07.015 CrossRefGoogle ScholarPubMed
Heilman, K.M., Rothi, L.J., & Valenstein, E. (1982). Two forms of ideomotor apraxia. Neurology, 32, 342–346.Google Scholar
Hodges, J.R., Bozeat, S., Lambon Ralph, M.A., Patterson, K., & Spatt, J. (2000). The role of conceptual knowledge in object use: Evidence from semantic dementia. Brain, 123, 1913–1925.Google Scholar
Hodges, J.R., Graham, N., & Patterson, K. (1995). Charting the progression in semantic dementia: Implications for the organisation of semantic memory. Memory, 3(3-4), 463–495. http://doi.org/10.1080/09658219508253161 CrossRefGoogle ScholarPubMed
Jarry, C., Osiurak, F., Delafuys, D., Chauviré, V., Etcharry-Bouyx, F., & Le Gall, D. (2013). Apraxia of tool use: More evidence for the technical reasoning hypothesis. Cortex, 49(9), 2322–2333. http://doi.org/10.1016/j.cortex.2013.02.011 Google Scholar
Kalénine, S., Buxbaum, L.J., & Coslett, H.B. (2010). Critical brain regions for action recognition: Lesion symptom mapping in left hemisphere stroke. Brain, 133(11), 3269–3280. http://doi.org/10.1093/brain/awq210 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.Google Scholar
Lesourd, M., Baumard, J., Jarry, C., Etcharry-Bouyx, F., Belliard, S., Moreaud, O., & Osiurak, F. (2016). Mechanical problem-solving strategies in Alzheimer’s disease and semantic dementia. Neuropsychology, 30(6), 612–623. http://doi.org/10.1037/neu0000241 CrossRefGoogle ScholarPubMed
Lesourd, M., Le Gall, D., Baumard, J., Croisile, B., Jarry, C., & Osiurak, F. (2013a). Apraxia and Alzheimer’s disease: Review and perspectives. Neuropsychology Review, 23(3), 234–256. http://doi.org/10.1007/s11065-013-9235-4 Google Scholar
Lesourd, M., Le Gall, D., Baumard, J., Croisile, B., Jarry, C., & Osiurak, F. (2013b). Apraxie et maladie d’Alzheimer. Revue de Neuropsychologie, 5(3), 213–222. http://doi.org/10.1684/nrp.2013.0273 Google Scholar
McDonald, S., Tate, R.L., & Rigby, J. (1994). Error types in ideomotor apraxia: A qualitative analysis. Brain and Cognition, 25(2), 250–270. http://doi.org/10.1006/brcg.1994.1035 Google Scholar
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939–944. http://doi.org/10.1212/WNL.34.7.939 Google Scholar
Negri, G.A., Lunardelli, A., Reverberi, C., Gigli, G.L., & Rumiati, R.I. (2007). Degraded semantic knowledge and accurate object use. Cortex, 43(3), 376–388. http://doi.org/10.1016/S0010-9452(08)70463-5 Google Scholar
Niessen, E., Fink, G.R., & Weiss, P.H. (2014). Apraxia, pantomime and the parietal cortex. Neuroimage: Clinical, 5, 42–52. http://doi.org/10.1016/j.nicl.2014.05.017 Google Scholar
Ochipa, C., Rothi, L.J.G., & Heilman, K.M. (1989). Ideational apraxia: A deficit in tool selection and use. Annals of Neurology, 25(2), 190–193. http://doi.org/10.1002/ana.410250214 CrossRefGoogle ScholarPubMed
Osiurak, F., & Badets, A. (2016). Tool use and affordance: Manipulation-based versus reasoning-based approaches. Psychological Review, [Epub ahead of print]. http://doi.org/10.1037/rev0000027 Google Scholar
Osiurak, F., Jarry, C., Allain, P., Aubin, G., Etcharry-Bouyx, F., Richard, I., & Le Gall, D. (2009). Unusual use of objects after unilateral brain damage. The technical reasoning model. Cortex, 45(6), 769–783. http://doi.org/10.1016/j.cortex.2008.06.013 Google Scholar
Osiurak, F., Jarry, C., & Le Gall, D. (2010). Grasping the affordances, understanding the reasoning: Toward a dialectical theory of human tool use. Psychological Review, 117(2), 517–540. http://doi.org/10.1037/a0019004 Google Scholar
Osiurak, F., Jarry, C., & Le Gall, D. (2011). Re-examining the gesture engram hypothesis. New perspectives on apraxia of tool use. Neuropsychologia, 49(3), 299–312. http://doi.org/10.1016/j.neuropsychologia.2010.12.041 Google Scholar
Poeck, K. (1983). Ideational apraxia. Journal of Neurology, 230(1), 1–5. http://doi.org/10.1007/BF00313591 Google Scholar
R Development Core Team. (2008). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.r-project.org Google Scholar
Reynaud, E., Lesourd, M., Navarro, J., & Osiurak, F. (2016). On the neurocognitive origins of human tool use a critical review of neuroimaging data. Neuroscience & Biobehavioral Reviews, 64, 421–437. http://doi.org/10.1016/j.neubiorev.2016.03.009 Google Scholar
Rothi, L.J.G., Ochipa, C., & Heilman, K.M. (1991). A cognitive neuropsychological model of limb praxis. Cognitive Neuropsychology, 8(6), 443–458. http://doi.org/10.1080/02643299108253382 Google Scholar
Signoret, J.L., Allard, M., Benoit, N., Bolgert, F., Bonvarlet, M., & Eustache, F. (1989). Batterie d’Evaluation Cognitive - BEC 96. Paris: Fondation IPSEN.Google Scholar
Vaina, L.M., & Jaulent, M.C. (1991). Object structure and action requirements: A compatibility model for functional recognition. International Journal of Intelligent Systems, 6, 313–336.Google Scholar
Vingerhoets, G., Vandekerckhove, E., Honoré, P., Vandemaele, P., & Achten, E. (2011). Neural correlates of pantomiming familiar and unfamiliar tools: Action semantics versus mechanical problem solving? Human Brain Mapping, 32(6), 905–918. http://doi.org/10.1002/hbm.21078 CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler Adult Intelligence Scale - 3rd Edition (WAIS-3). San Antonio: TX: Harcourt Assessment.Google Scholar
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