Exploring manual asymmetries during grasping: a dynamic causal modeling approach

Recording of neural activity during grasping actions in macaques showed that grasp-related sensorimotor transformations are accomplished in a circuit constituted by the anterior part of the intraparietal sulcus (AIP), the ventral (F5) and the dorsal (F2) region of the premotor area. In humans, neuroimaging studies have revealed the existence of a similar circuit, involving the putative homolog of macaque areas AIP, F5, and F2. These studies have mainly considered grasping movements performed with the right dominant hand and only a few studies have measured brain activity associated with a movement performed with the left non-dominant hand. As a consequence of this gap, how the brain controls for grasping movement performed with the dominant and the non-dominant hand still represents an open question. A functional magnetic resonance imaging (fMRI) experiment has been conducted, and effective connectivity (dynamic causal modeling, DCM) was used to assess how connectivity among grasping-related areas is modulated by hand (i.e., left and right) during the execution of grasping movements toward a small object requiring precision grasping. Results underlined boosted inter-hemispheric couplings between dorsal premotor cortices during the execution of movements performed with the left rather than the right dominant hand. More specifically, they suggest that the dorsal premotor cortices may play a fundamental role in monitoring the configuration of fingers when grasping movements are performed by either the right and the left hand. This role becomes particularly evident when the hand less-skilled (i.e., the left hand) to perform such action is utilized. The results are discussed in light of recent theories put forward to explain how parieto-frontal connectivity is modulated by the execution of prehensile movements.

[1]  D. Schwartz,et al.  The Role of Parents , 2015 .

[2]  A. Lingnau,et al.  Neural correlates of grasping , 2014, Front. Hum. Neurosci..

[3]  U. Castiello,et al.  An investigation of the neural circuits underlying reaching and reach-to-grasp movements: from planning to execution , 2014, Front. Hum. Neurosci..

[4]  Takemi Otsuki,et al.  Functional Properties of CD8+ Lymphocytes in Patients with Pleural Plaque and Malignant Mesothelioma , 2014, Journal of immunology research.

[5]  D. Kourtis,et al.  Handedness consistency influences bimanual coordination: A behavioural and electrophysiological investigation , 2014, Neuropsychologia.

[6]  Yun Qu,et al.  Effects of Repetitive Transcranial Magnetic Stimulation on Hand Function Recovery and Excitability of the Motor Cortex After Stroke: A Meta-Analysis , 2014, American journal of physical medicine & rehabilitation.

[7]  Xueliang Li,et al.  On a Relation Between , 2012 .

[8]  Scott H. Frey,et al.  Handedness-dependent and -independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning , 2011, NeuroImage.

[9]  Cathy J. Price,et al.  Lateralization is Predicted by Reduced Coupling from the Left to Right Prefrontal Cortex during Semantic Decisions on Written Words , 2010, Cerebral cortex.

[10]  Flavia Filimon Human Cortical Control of Hand Movements: Parietofrontal Networks for Reaching, Grasping, and Pointing , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[11]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[12]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[13]  U. Castiello,et al.  Cortical Activations in Humans Grasp-Related Areas Depend on Hand Used and Handedness , 2008, PloS one.

[14]  K. Amunts,et al.  Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. , 2008, Cerebral cortex.

[15]  Umberto Castiello,et al.  The Cortical Control of Visually Guided Grasping , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[16]  Scott Barbay,et al.  Interhemispheric connections of the ventral premotor cortex in a new world primate , 2007, The Journal of comparative neurology.

[17]  Karl J. Friston,et al.  Comparing hemodynamic models with DCM , 2007, NeuroImage.

[18]  Wolfgang Grodd,et al.  Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping , 2007, PloS one.

[19]  Ivan Toni,et al.  Parieto-Frontal Connectivity during Visually Guided Grasping , 2007, The Journal of Neuroscience.

[20]  Emily S. Cross,et al.  On-line grasp control is mediated by the contralateral hemisphere , 2007, Brain Research.

[21]  Robert L. Whitwell,et al.  Left handedness does not extend to visually guided precision grasping , 2007, Experimental Brain Research.

[22]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[23]  T Brochier,et al.  Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. , 2007, Journal of neurophysiology.

[24]  M. Goodale,et al.  FMRI Reveals a Dissociation between Grasping and Perceiving the Size of Real 3D Objects , 2007, PloS one.

[25]  M. Davare,et al.  Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area , 2007, The Journal of Neuroscience.

[26]  U. Castiello,et al.  Differential cortical activity for precision and whole‐hand visually guided grasping in humans , 2007, The European journal of neuroscience.

[27]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[28]  A. Schnitzler,et al.  Asymmetry of interhemispheric interaction in left-handed subjects , 2006, Experimental Brain Research.

[29]  Scott T Grafton,et al.  The Anterior Intraparietal Sulcus Mediates Grasp Execution, Independent of Requirement to Update: New Insights from Transcranial Magnetic Stimulation , 2006, The Journal of Neuroscience.

[30]  T. Vecchi,et al.  Handedness effects on interhemispheric transfer time: A TMS study , 2006, Brain Research Bulletin.

[31]  Tzvi Ganel,et al.  Hemispheric specialization for the visual control of action is independent of handedness. , 2006, Journal of neurophysiology.

[32]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[33]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

[34]  M. Davare,et al.  Behavioral / Systems / Cognitive Dissociating the Role of Ventral and Dorsal Premotor Cortex in Precision Grasping , 2018 .

[35]  U. Castiello The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[36]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

[37]  Scott T. Grafton,et al.  Cortical topography of human anterior intraparietal cortex active during visually guided grasping. , 2005, Brain research. Cognitive brain research.

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

[39]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[40]  L. Fogassi,et al.  Functional properties of grasping-related neurons in the dorsal premotor area F2 of the macaque monkey. , 2004, Journal of neurophysiology.

[41]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[42]  Eli Brenner,et al.  On the relation between object shape and grasping kinematics. , 2004, Journal of neurophysiology.

[43]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[44]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[45]  Claudio Babiloni,et al.  Hemispherical Asymmetry in Human SMA During Voluntary Simple Unilateral Movements. An fMRI Study , 2003, Cortex.

[46]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

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

[48]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

[49]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[50]  Vittorio Gallese,et al.  Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. , 2003, Journal of neurophysiology.

[51]  S. Small,et al.  Functional Lateralization of the Human Premotor Cortex during Sequential Movements , 2002, Brain and Cognition.

[52]  J. Sanes,et al.  Improved Detection of Event-Related Functional MRI Signals Using Probability Functions , 2001, NeuroImage.

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

[54]  Ivan Toni,et al.  Movement Preparation and Motor Intention , 2001, NeuroImage.

[55]  Martin V. Sale,et al.  Asymmetry of motor cortex excitability during a simple motor task: relationships with handedness and manual performance , 2001, Experimental Brain Research.

[56]  Karl J. Friston,et al.  The choice of basis functions in event-related fMRI , 2001, NeuroImage.

[57]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[58]  K. Amunts,et al.  Interhemispheric asymmetry of the human motor cortex related to handedness and gender , 2000, Neuropsychologia.

[59]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[60]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[61]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[62]  Carlo Adolfo Porro,et al.  Bilateral representation of sequential finger movements in human cortical areas , 1999, Neuroscience Letters.

[63]  E. Brenner,et al.  A new view on grasping. , 1999, Motor control.

[64]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[65]  A Schnitzler,et al.  Handedness and asymmetry of hand representation in human motor cortex. , 1998, Journal of neurophysiology.

[66]  G. Rizzolatti,et al.  Grasping objects and grasping action meanings: the dual role of monkey rostroventral premotor cortex (area F5). , 1998, Novartis Foundation symposium.

[67]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[68]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[69]  A. Schleicher,et al.  Asymmetry in the Human Motor Cortex and Handedness , 1996, NeuroImage.

[70]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[71]  Kevin W. Bowyer,et al.  The Functional Properties , 1996 .

[72]  G. Savelsbergh,et al.  The role of fragility information in the guidance of the precision grip , 1996 .

[73]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[74]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[75]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[76]  D. Boussaoud Primate premotor cortex: modulation of preparatory neuronal activity by gaze angle. , 1995, Journal of neurophysiology.

[77]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[78]  Ira B. Perelle,et al.  An international study of human handedness: The data , 1994, Behavior genetics.

[79]  S. Kinomura,et al.  Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement , 1993, Brain Research.

[80]  Umberto Castiello,et al.  The bilateral reach to grasp movement , 1993, Behavioural Brain Research.

[81]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[82]  L. Binder Hemispheric specialization. , 1988, The Psychiatric clinics of North America.

[83]  G. Leichnetz Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8 , 1986, The Journal of comparative neurology.

[84]  N. Geschwind,et al.  Handedness is not a Unidimensional Trait , 1986, Cortex.

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

[86]  M. Jeannerod Intersegmental coordination during reaching at natural visual objects , 1981 .

[87]  A. Jenny Commissural projections of the cortical hand motor area in monkeys , 1979, The Journal of comparative neurology.

[88]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.