The neural basis of tool use.

Misuse of tools and objects by patients with left brain damage is generally recognized as a manifestation of apraxia, caused by parietal lobe damage. The use of tools and objects can, however, be subdivided in several components. The purpose of our study was to find out which of these are dependent on parietal lobe function. Thirty-eight patients with left brain damage and aphasia were examined using tests to assess the retrieval of functional knowledge from semantic memory (Functional Associations), mechanical problem solving (Novel Tools) and use of everyday tools and objects (Common Tools). Voxel-wise analysis of magnetic resonance images revealed two regions where lesions had a significant impact on the test results. One extended rostrally from the central region and ventrally through the middle frontal cortex to the dorsal margin of the inferior frontal gyrus. The other reached dorsally and caudally from the supramarginal gyrus, through the inferior, to superior parietal lobe. Whereas the frontal lesions had an adverse influence on all experimental tests as well as on the subtests of the Aachen Aphasia test, parietal lesions impaired Novel and Common Tools, but did not have an adverse effect on the Functional Associates. An association between Functional Associations and temporal lesions became apparent when patients with only a selective deficit in the test were considered, but did not show up in the whole group analysis. The parietal influence was as strong for the selection as for the use of either novel or common tools, although choice of appropriate manual configuration and movements was more important for use than for selection. We conclude that the contribution of the parietal lobe to tool use concerns general principles of tool use rather than knowledge about the prototypical use of common tools and objects, and the comprehension of mechanical interactions of the tool with other tools, recipients or material rather than the selection of grip formation and manual movements.

[1]  E. Renzi,et al.  Ideational apraxia: A quantitative study , 1968 .

[2]  H. Steinthal Abriss der Sprachwissenschaft , 1972 .

[3]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[4]  [The syndrome of ideational apraxia and its localisation]. , 1980, Der Nervenarzt.

[5]  T. Shallice Specific impairments of planning. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  Colin Potts,et al.  Design of Everyday Things , 1988 .

[7]  Richard J. Brown Neuropsychology Mental Structure , 1989 .

[8]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[9]  John Hart,et al.  Delineation of single‐word semantic comprehension deficits in aphasia, with anatomical correlation , 1990, Annals of neurology.

[10]  M Poncet,et al.  The role of sensorimotor experience in object recognition. A case of multimodal agnosia. , 1991, Brain : a journal of neurology.

[11]  Marie-Christine Jaulent,et al.  Object structure and action requirements: A compatibility model for functional recognition , 1991, Int. J. Intell. Syst..

[12]  K M Heilman,et al.  Conceptual apraxia in Alzheimer's disease. , 1992, Brain : a journal of neurology.

[13]  J. Fuster Frontal lobes , 1993, Current Opinion in Neurobiology.

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

[15]  G. Gainotti,et al.  Neuroanatomical correlates of category-specific semantic disorders: a critical survey. , 1995, Memory.

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

[17]  K M Heilman,et al.  Ecological implications of limb apraxia: Evidence from mealtime behavior , 1995, Journal of the International Neuropsychological Society.

[18]  A. Damasio,et al.  A neural basis for lexical retrieval , 1996, Nature.

[19]  R. Cabeza,et al.  Imaging Cognition: An Empirical Review of PET Studies with Normal Subjects , 1997, Journal of Cognitive Neuroscience.

[20]  K M Heilman,et al.  Conceptual apraxia from lateralized lesions , 1997, Neurology.

[21]  Michael W. Montgomery,et al.  Naturalistic action impairment in closed head injury. , 1998, Neuropsychology.

[22]  G. Goldenberg,et al.  Tool use and mechanical problem solving in apraxia , 1998, Neuropsychologia.

[23]  G. Humphreys,et al.  Disordered action schema and action disorganisation syndrome , 1998 .

[24]  Laurel J Buxbaum,et al.  Naturalistic action production following right hemisphere stroke , 1998, Neuropsychologia.

[25]  J R Hodges,et al.  "What" and "how": evidence for the dissociation of object knowledge and mechanical problem-solving skills in the human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Hermsdörfer,et al.  Effects of unilateral brain damage on grip selection, coordination, and kinematics of ipsilesional prehension , 1999, Experimental Brain Research.

[27]  A. Sunderland,et al.  Impaired dexterity of the ipsilateral hand after stroke and the relationship to cognitive deficit. , 1999, Stroke.

[28]  M. L. Lambon Ralph,et al.  The role of conceptual knowledge in object use evidence from semantic dementia. , 2000, Brain : a journal of neurology.

[29]  M P Young,et al.  On imputing function to structure from the behavioural effects of brain lesions. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[31]  Using a fixed provisional as an orthodontic anchor in forced eruption. , 2000, Practical periodontics and aesthetic dentistry : PPAD.

[32]  Alex Martin,et al.  Representation of Manipulable Man-Made Objects in the Dorsal Stream , 2000, NeuroImage.

[33]  H. Freund,et al.  Recognition and imitation of pantomimed motor acts after unilateral parietal and premotor lesions: a perspective on apraxia , 2001, Neuropsychologia.

[34]  T Shallice,et al.  A Form of Ideational Apraxia as a Delective Deficit of Contention Scheduling , 2001, Cognitive neuropsychology.

[35]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

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

[37]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[38]  T. Fukutake,et al.  Apraxia of Tool Use: An Autopsy Case of Biparietal Infarction , 2002, European Neurology.

[39]  J. Decety,et al.  Does visual perception of object afford action? Evidence from a neuroimaging study , 2002, Neuropsychologia.

[40]  Karalyn Patterson,et al.  Apraxia, mechanical problem solving and semantic knowledge: contributions to object usage in corticobasal degeneration. , 2002, Journal of neurology.

[41]  J. Hodges,et al.  When objects lose their meaning: What happens to their use? , 2002, Cognitive, affective & behavioral neuroscience.

[42]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[43]  R. Adolphs,et al.  NEURAL CORRELATES OF CONCEPTUAL KNOWLEDGE FOR ACTIONS , 2003, Cognitive neuropsychology.

[44]  M. Brett,et al.  Actions Speak Louder Than Functions: The Importance of Manipulability and Action in Tool Representation , 2003, Journal of Cognitive Neuroscience.

[45]  D. Povinelli Folk physics for apes : the chimpanzee's theory of how the world works , 2003 .

[46]  M. Hegarty Mechanical reasoning by mental simulation , 2004, Trends in Cognitive Sciences.

[47]  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.

[48]  K. Poeck Ideational apraxia , 2004, Journal of Neurology.

[49]  Sergio E Chaigneau,et al.  Assessing the causal structure of function. , 2004, Journal of experimental psychology. General.

[50]  R. Rumiati Right, left or both? Brain hemispheres and apraxia of naturalistic actions , 2005, Trends in Cognitive Sciences.

[51]  L. Buxbaum,et al.  Distinctions between manipulation and function knowledge of objects: evidence from functional magnetic resonance imaging. , 2005, Brain research. Cognitive brain research.

[52]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  Ueber „subcorticale“ Alexie mit Agraphie und Apraxie , 1903, Deutsche Zeitschrift für Nervenheilkunde.

[54]  J. Hermsdörfer,et al.  It takes the whole brain to make a cup of coffee: the neuropsychology of naturalistic actions involving technical devices , 2005, Neuropsychologia.

[55]  F. Lacquaniti,et al.  Cognitive, perceptual and action-oriented representations of falling objects , 2005, Neuropsychologia.

[56]  M. Catani,et al.  The rises and falls of disconnection syndromes. , 2005, Brain : a journal of neurology.

[57]  A. Sirigu,et al.  How we interact with objects: learning from brain lesions , 2006, Trends in Cognitive Sciences.

[58]  JamesW. Lewis Cortical Networks Related to Human Use of Tools , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[59]  Alan Sunderland,et al.  Ideomotor Apraxia And Functional Ability , 2007, Cortex.

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

[61]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[62]  G. Gigli,et al.  Degraded Semantic Knowledge And Accurate Object Use , 2007, Cortex.

[63]  G. Goldenberg,et al.  The Impact of Dysexecutive Syndrome on Use of Tools and Technical Devices , 2007, Cortex.

[64]  Claudio Babiloni,et al.  Human neural systems for conceptual knowledge of proper object use: a functional magnetic resonance imaging study. , 2007, Cerebral cortex.

[65]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[66]  F. Osiurak,et al.  Different constraints on grip selection in brain-damaged patients: Object use versus object transport , 2008, Neuropsychologia.

[67]  Tim Shallice,et al.  The different neural correlates of action and functional knowledge in semantic memory: an FMRI study. , 2008, Cerebral cortex.

[68]  G. Goldenberg,et al.  Neuropsychology and behavioral neurology , 2008 .

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

[70]  F. Osiurak,et al.  Unusual use of objects after unilateral brain damage. The technical reasoning model , 2009, Cortex.

[71]  Frank Marchak,et al.  Constraints for Action Selection: Overhand Versus Underhand Grips , 2018, Attention and Performance XIII.