Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping

Background Neurophysiological studies showed that in macaques, grasp-related sensorimotor transformations are accomplished in a circuit connecting the anterior intraparietal sulcus (area AIP) with premotor area F5. Single unit recordings of macaque indicate that activity of neurons in this circuit is not simply linked to any particular object. Instead, responses correspond to the final hand configuration used to grasp the object. Although a human homologue of such a circuit has been identified, its role in planning and controlling different grasp configurations has not been decisively shown. We used functional magnetic resonance imaging to explicitly test whether activity within this network varies depending on the congruency between the adopted grasp and the grasp called by the stimulus. Methodology/Principal Findings Subjects were requested to reach towards and grasp a small or a large stimulus naturally (i.e., precision grip, involving the opposition of index finger and thumb, for a small size stimulus and a whole hand grasp for a larger stimulus) or with an constrained grasp (i.e., a precision grip for a large stimulus and a whole hand grasp for a small stimulus). The human anterior intraparietal sulcus (hAIPS) was more active for precise grasping than for whole hand grasp independently of stimulus size. Conversely, both the dorsal premotor cortex (dPMC) and the primary motor cortex (M1) were modulated by the relationship between the type of grasp that was adopted and the size of the stimulus. Conclusions/Significance The demonstration that activity within the hAIPS is modulated according to different types of grasp, together with the evidence in humans that the dorsal premotor cortex is involved in grasp planning and execution offers a substantial contribution to the current debate about the neural substrates of visuomotor grasp in humans.

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

[2]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

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

[4]  U. Castiello,et al.  Reach to grasp: the natural response to perturbation of object size , 2004, Experimental Brain Research.

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

[6]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[7]  Hans Forssberg,et al.  Human brain activity in the control of fine static precision grip forces: an fMRI study , 2001, The European journal of neuroscience.

[8]  R. Lemon,et al.  Corticospinal neurons with a special role in precision grip , 1983, Brain Research.

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

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

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

[12]  John D. E. Gabrieli,et al.  Material-dependent and material-independent selection processes in the frontal and parietal lobes: an event-related fMRI investigation of response competition , 2003, Neuropsychologia.

[13]  H. Sakata,et al.  Hand-Movement-Related Neurons of the Posterior Parietal Cortex of the Monkey: Their Role in the Visual Guidance of Hand Movements , 1992 .

[14]  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.

[15]  L. Fogassi,et al.  Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. , 2006, Journal of neurophysiology.

[16]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[17]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

[18]  G. Rizzolatti,et al.  Influence of different types of grasping on the transport component of prehension movements , 1991, Neuropsychologia.

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

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

[21]  R. Lemon,et al.  Variety of functional organization within the monkey motor cortex , 1981, The Journal of physiology.

[22]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

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

[24]  H. Forssberg,et al.  Simultaneous movements of upper and lower limbs are coordinated by motor representations that are shared by both limbs: a PET study , 2000, The European journal of neuroscience.

[25]  R. Lemon,et al.  Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. , 1986, The Journal of physiology.

[26]  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.

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

[28]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[29]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

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

[31]  T. Ebner,et al.  Representation of accuracy in the dorsal premotor cortex , 2000, The European journal of neuroscience.

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

[33]  T J Ebner,et al.  Primary motor cortex neuronal discharge during reach-to-grasp: controlling the hand as a unit. , 2002, Archives italiennes de biologie.

[34]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[35]  Umberto Castiello,et al.  How perceived object dimension influences prehension , 1996, Neuroreport.

[36]  R. Porter,et al.  Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

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

[39]  Karl J. Friston,et al.  Correcting for non-sphericity in imaging data using classical and Bayesian approaches , 2001, NeuroImage.

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

[41]  John Dickinson The hand: a philosophical inquiry into human being , 2005 .

[42]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

[43]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[45]  D Yves von Cramon,et al.  Premotor cortex in observing erroneous action: an fMRI study. , 2003, Brain research. Cognitive brain research.

[46]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[47]  R N Lemon,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993, Experimental physiology.

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

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

[50]  A. Georgopoulos,et al.  Parietal cortex neurons of the monkey related to the visual guidance of hand movement , 1990, Experimental Brain Research.

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

[52]  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 .

[53]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[54]  M. M. Morrow,et al.  Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. , 2003, Journal of neurophysiology.

[55]  Roberto Caminiti,et al.  Control of arm movement in space : neurophysiological and computational approaches , 1992 .

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