Different left brain regions are essential for grasping a tool compared with its subsequent use

Tool use engages a left hemispheric network including frontal, temporal and parietal regions. Patients with left brain lesions (LBD patients) exhibit deficits when demonstrating use of a single tool (apraxia). When attempting to use a tool, some apraxic patients show errors in the preceding grasping movement. Forty-two LBD patients and 18 healthy controls grasped individual tools and demonstrated their typical use. For patients with a tool use impairment (22), lesion analysis revealed a large area of overlap in the left hemisphere, mainly in the supramarginal gyrus (SMG). For patients with erroneous grasping (12), the lesion overlay showed overlaps in the left frontal and parietal cortices, especially in the inferior frontal gyrus (IFG) and the angular gyrus (ANG). However, contrasting lesions associated with impaired grasping versus tool use impairments reveal little overlap, limited to the inferior parietal cortex. Presumably the left IFG is involved in selection processes in the context of tool use, such as choosing a functional or non-functional grasping movement depending on the task and the online information about the tool's structure and orientation. The ANG might provide this grasp related information, which is relevant for the specific action. The contribution of the SMG to tool use involves more general principals, such as integrating online and learned tool use information into the action plan for the use movement.

[1]  Eugene Tunik,et al.  Transcranial Magnetic Stimulation to the Frontal Operculum and Supramarginal Gyrus Disrupts Planning of Outcome-Based Hand–Object Interactions , 2008, The Journal of Neuroscience.

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

[3]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[4]  Georg Goldenberg,et al.  Chapter 16 Apraxia , 2008 .

[5]  Marc Jeannerod.  Motor representation and control , 1990 .

[6]  Hans Forssberg,et al.  Phonological working memory with auditory presentation of pseudo-words — An event related fMRI Study , 2008, Brain Research.

[7]  S. Frey.  Tool use, communicative gesture and cerebral asymmetries in the modern human brain , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[9]  D. Rosenbaum,et al.  Planning for manual positioning: the end-state comfort effect for manual abduction–adduction , 2007, Experimental Brain Research.

[10]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

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

[12]  Scott T Grafton,et al.  Repetition suppression for performed hand gestures revealed by fMRI , 2009, Human brain mapping.

[13]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

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

[15]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

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

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

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

[19]  Gereon R. Fink,et al.  Functional Interactions during the Retrieval of Conceptual Action Knowledge: An fMRI Study , 2007, Journal of Cognitive Neuroscience.

[20]  Joseph S. Gati,et al.  Visually-guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2010 .

[21]  M. Gentilucci,et al.  Planning for action , 2020, Coaching with Research in Mind.

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

[23]  Scott T Grafton,et al.  Differential Recruitment of Anterior Intraparietal Sulcus and Superior Parietal Lobule during Visually Guided Grasping Revealed by Electrical Neuroimaging , 2008, The Journal of Neuroscience.

[24]  Matthew F. S. Rushworth,et al.  Parietal rTMS Disrupts the Initiation but not the Execution of On-line Adjustments to a Perturbation of Object Size , 2005, Journal of Cognitive Neuroscience.

[25]  A. Murata,et al.  Cortical connections of the macaque anterior intraparietal (AIP) area. , 2008, Cerebral cortex.

[26]  Chris Rorden,et al.  Lesion Mapping of Cognitive Abilities Linked to Intelligence , 2009, Neuron.

[27]  Afdc Hamilton,et al.  The motor hierarchy: from kinematics to goals and intentions , 2007 .

[28]  L. Buxbaum,et al.  Knowledge of object manipulation and object function: dissociations in apraxic and nonapraxic subjects , 2002, Brain and Language.

[29]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[30]  Sarah H. Creem,et al.  Grasping objects by their handles: a necessary interaction between cognition and action. , 2001, Journal of experimental psychology. Human perception and performance.

[31]  J. Hermsdörfer,et al.  Grasping tools: Effects of task and apraxia , 2009, Neuropsychologia.

[32]  Scott T. Grafton,et al.  Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp , 2005, Nature Neuroscience.

[33]  G. Goldenberg,et al.  The neural basis of tool use. , 2009, Brain : a journal of neurology.

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

[35]  Eric Achten,et al.  Tool responsive regions in the posterior parietal cortex: Effect of differences in motor goal and target object during imagined transitive movements , 2009, NeuroImage.

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

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

[38]  Scott T. Grafton,et al.  Premotor Cortex Activation during Observation and Naming of Familiar Tools , 1997, NeuroImage.

[39]  L. Buxbaum,et al.  Action knowledge, visuomotor activation, and embodiment in the two action systems , 2010, Annals of the New York Academy of Sciences.

[40]  M. Jeannerod.  The timing of natural prehension movements. , 1984, Journal of motor behavior.

[41]  Ravi S. Menon,et al.  Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2003, Experimental Brain Research.

[42]  Alex Martin,et al.  A neural system for learning about object function. , 2006, Cerebral cortex.

[43]  Thomas E. Nichols,et al.  Rank-order versus mean based statistics for neuroimaging , 2007, NeuroImage.

[44]  Alex Martin,et al.  Grounding Object Concepts in Perception and Action: Evidence from FMRI Studies of Tools , 2007, Cortex.

[45]  Edward E. Smith,et al.  The Neural Basis for Categorization in Semantic Memory , 2002, NeuroImage.

[46]  M. Short,et al.  Planning macroscopic aspects of manual control: end-state comfort and point-of-change effects. , 1997, Acta psychologica.

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

[48]  J. Hermsdörfer,et al.  Neural representations of pantomimed and actual tool use: Evidence from an event-related fMRI study , 2007, NeuroImage.

[49]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[50]  M. Jeannerod,et al.  Constraints on human arm movement trajectories. , 1987, Canadian journal of psychology.

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

[52]  Wolfgang Weinrich,et al.  Klinische Neuroanatomie und kranielle Bilddiagnostik , 2007 .

[53]  James N. Lee,et al.  The influence of complex action knowledge on representations of novel graspable objects: Evidence from functional magnetic resonance imaging , 2007, Journal of the International Neuropsychological Society.

[54]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

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

[56]  R L Klatzky,et al.  Planning for hand shape and arm transport when reaching for objects. , 1995, Acta psychologica.

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

[58]  C. Armbrüster,et al.  Movement planning in prehension: do intended actions influence the initial reach and grasp movement? , 2006, Motor control.