Functional imaging of the parietal cortex during action execution and observation.

We used the (14)C-deoxyglucose method to map the functional activity in the cortex of the lateral and medial parietal convexity, the intraparietal and the parietoccipital sulci of monkeys which either reached and grasped a 3D-object or observed the same reaching-to-grasp movements executed by a human. Execution of reaching-to-grasp induced activations in the superior parietal areas SI-forelimb/convexity, PE, PE caudal (PEc); in the intraparietal areas PE intraparietal (PEip), medial intraparietal (MIP), 5 intraparietal posterior, ventral intraparietal (VIP), anterior intraparietal (AIP), lateral intraparietal dorsal; in the inferior parietal areas PF, PFG, PG; in the parietoccipital areas V6, V6A-dorsal; in the medial cortical areas PGm/7m and retrosplenial cortex. Observation of reaching-to-grasp activated areas SI-forelimb/convexity, PE lateral, PEc, PEip, MIP, VIP, AIP, PF, V6, PGm/7m, 31, and retrosplenial cortex. The common activations were stronger for execution than for observation and the interhemispheric differences were smaller for observation than for execution, contributing to the attribution of action to the correct agent. The extensive overlap of parietal networks activated for action execution and observation supports the "mental simulation theory" which assigns the role of understanding others' actions to the entire distributed neural network responsible for the execution of actions, and not the concept of "mirroring" which reflects the function of a certain class of cells in a couple of cortical areas.

[1]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[2]  Ehud Zohary,et al.  A Mirror Representation of Others' Actions in the Human Anterior Parietal Cortex , 2006, The Journal of Neuroscience.

[3]  L. Sokoloff,et al.  Local cerebral glucose utilization in the normal conscious macaque monkey , 1978, Annals of neurology.

[4]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[5]  Natalie Sebanz,et al.  Simulation, mirroring, and a different argument from error , 2005, Trends in Cognitive Sciences.

[6]  G. G. Gregoriou,et al.  Functional imaging of the intraparietal cortex during saccades to visual and memorized targets , 2006, NeuroImage.

[7]  J. D. Crawford,et al.  Eye-hand Coordination During Reaching in 3D Space: Binocular Fixation and Internal Models , 2002 .

[8]  Peter Janssen,et al.  Anterior Regions of Monkey Parietal Cortex Process Visual 3D Shape , 2007, Neuron.

[9]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[10]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

[11]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[12]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[13]  T. P. S. Powell,et al.  The projection of the primary somatic sensory cortex upon area 5 in the monkey , 1985, Brain Research Reviews.

[14]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[15]  C. Galletti,et al.  Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto‐occipital sulcus of the macaque: a cytoarchitectonic study , 2005, The European journal of neuroscience.

[16]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[17]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

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

[19]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[20]  Paul B. Johnson,et al.  The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. , 1996, Cerebral cortex.

[21]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[22]  S. Stine,et al.  Extreme and persistent drought in California and Patagonia during mediaeval time , 1994, Nature.

[23]  C. Galletti,et al.  Spatial tuning of reaching activity in the medial parieto‐occipital cortex (area V6A) of macaque monkey , 2005, The European journal of neuroscience.

[24]  Georgia G Gregoriou,et al.  When vision guides movement: a functional imaging study of the monkey brain , 2003, NeuroImage.

[25]  P. Haggard,et al.  Altered awareness of voluntary action after damage to the parietal cortex , 2004, Nature Neuroscience.

[26]  C. Galletti,et al.  Functional Demarcation of a Border Between Areas V6 and V6A in the Superior Parietal Gyrus of the Macaque Monkey , 1996, The European journal of neuroscience.

[27]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[28]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[29]  C. Galletti,et al.  Role of the medial parieto-occipital cortex in the control of reaching and grasping movements , 2003, Experimental Brain Research.

[30]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

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

[32]  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.

[33]  E Vaudano,et al.  Injury induced c‐Jun expression and phosphorylation in the dopaminergic nigral neurons of the rat: correlation with neuronal death and modulation by glial‐cell‐line‐derived neurotrophic factor , 2001, The European journal of neuroscience.

[34]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[35]  Daniel M. Wolpert,et al.  Where does your own action influence your perception of another person's action in the brain? , 2006, NeuroImage.

[36]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[37]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[38]  Michael L Platt,et al.  Visual and saccade-related activity in macaque posterior cingulate cortex. , 2004, Journal of neurophysiology.

[39]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[40]  A. Murata,et al.  Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4) , 1999, Experimental Brain Research.

[41]  A. Sirigu,et al.  The Mental Representation of Hand Movements After Parietal Cortex Damage , 1996, Science.

[42]  C Galletti,et al.  Superior area 6 afferents from the superior parietal lobule in the macaque monkey , 1998, The Journal of comparative neurology.

[43]  齋藤 大輔,et al.  Tactile-visual cross-modal shape matching : A functional MRI study , 2003 .

[44]  H. Barbas,et al.  Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure , 2006, The European journal of neuroscience.

[45]  V. Raos,et al.  Spatial cortical patterns of metabolic activity in monkeys performing a visually guided reaching task with one forelimb , 1997, Neuroscience.

[46]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[47]  F. Lacquaniti,et al.  Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. , 2001, Cerebral cortex.

[48]  F. Lacquaniti,et al.  Visual Control of Hand‐reaching Movement: Activity in Parietal Area 7m , 1997, The European journal of neuroscience.

[49]  C. Galletti,et al.  Evidence for both reaching and grasping activity in the medial parieto‐occipital cortex of the macaque , 2004, The European journal of neuroscience.

[50]  Helen E. Savaki,et al.  Observation of action: grasping with the mind's hand , 2004, NeuroImage.

[51]  C. Gross,et al.  Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: A dual tracer study , 1988, The Journal of comparative neurology.

[52]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[53]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[54]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[55]  R. Andersen Visual and eye movement functions of the posterior parietal cortex. , 1989, Annual review of neuroscience.

[56]  G. Sheean,et al.  Upper Motor Neurone Syndrome and Spasticity: Neurophysiology of spasticity , 2008 .

[57]  P. B. Cipolloni,et al.  Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey , 2004, The Journal of comparative neurology.

[58]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[59]  M Mishkin,et al.  Visually guided reaching with the forelimb contralateral to a "blind" hemisphere: a metabolic mapping study in monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  C. Galletti,et al.  The cortical connections of area V6: an occipito‐parietal network processing visual information , 2001, The European journal of neuroscience.

[61]  Hideo Sakata,et al.  Short-Term Memory and Perceptual Decision for Three-Dimensional Visual Features in the Caudal Intraparietal Sulcus (Area CIP) , 2003, The Journal of Neuroscience.

[62]  M. Jeannerod,et al.  Perception of self-generated movement following left parietal lesion. , 1999, Brain : a journal of neurology.

[63]  C. Galletti,et al.  Neuronal mechanisms for detection of motion in the field of view , 2003, Neuropsychologia.

[64]  J. Kalaska,et al.  Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics , 2004, Experimental Brain Research.

[65]  S. Blakemore,et al.  Motor activation prior to observation of a predicted movement , 2004, Nature Neuroscience.

[66]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[67]  J. Kalaska Parietal cortex area 5 and visuomotor behavior. , 1996, Canadian journal of physiology and pharmacology.

[68]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[69]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[70]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[71]  M Petrides,et al.  Architecture and connections of retrosplenial area 30 in the rhesus monkey (macaca mulatta). , 1999, The European journal of neuroscience.

[72]  V. Raos,et al.  Metabolic activity pattern in the motor and somatosensory cortex of monkeys performing a visually guided reaching task with one forelimb , 1996, Neuroscience.

[73]  C. Galletti,et al.  Brain location and visual topography of cortical area V6A in the macaque monkey , 1999, The European journal of neuroscience.

[74]  P. Haggard,et al.  Voluntary action and conscious awareness , 2002, Nature Neuroscience.

[75]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[76]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[77]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[78]  V. Raos,et al.  Mental Simulation of Action in the Service of Action Perception , 2007, The Journal of Neuroscience.

[79]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[80]  Romeo Chua,et al.  Asymmetries in the spatial localization of transformed targets , 1992, Brain and Cognition.

[81]  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.

[82]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[83]  S. Zeki,et al.  A visuo‐somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A , 1998, The European journal of neuroscience.

[84]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[85]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

[86]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

[87]  J. Decety Do imagined and executed actions share the same neural substrate? , 1996, Brain research. Cognitive brain research.

[88]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

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

[90]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[91]  S. Blakemore,et al.  Delusions of alien control in the normal brain , 2003, Neuropsychologia.

[92]  M. Mascaro,et al.  Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. , 2007, Cerebral cortex.

[93]  J. Danckert Common Mechanisms in Perception and Action: Attention and Performance XIX Wolfgang Prinz, Bernhard Hommel (Eds.), Oxford University Press, 2002, Price: £ 65.00, ISBN: 0-19-851069 , 2003, Neuropsychologia.

[94]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

[95]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Elena Borra,et al.  Architectonic organization of the inferior parietal convexity of the macaque monkey , 2006, The Journal of comparative neurology.

[97]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[98]  Lauretta Passarelli,et al.  Somatosensory Cells in Area PEc of Macaque Posterior Parietal Cortex , 2006, The Journal of Neuroscience.

[99]  Gian Luca Romani,et al.  Neural systems underlying observation of humanly impossible movements: an FMRI study. , 2005, Cerebral cortex.

[100]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[101]  J. F. Kalaska,et al.  Parietal corte× area 5 and visuomotor behavior , 1996 .

[102]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[103]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[104]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[105]  Helen E. Savaki,et al.  14C-Deoxyglucose mapping of the monkey brain during reaching to visual targets , 1999, Progress in Neurobiology.

[106]  G. G. Gregoriou,et al.  Frontal cortical areas of the monkey brain engaged in reaching behavior: A 14C-deoxyglucose imaging study , 2005, NeuroImage.

[107]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[108]  Jessie Chen,et al.  Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors. , 2007, Journal of neurophysiology.

[109]  Michela Gamberini,et al.  ‘Arm‐reaching’ neurons in the parietal area V6A of the macaque monkey , 2001, The European journal of neuroscience.

[110]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[111]  Patrick Haggard,et al.  Motor awareness without perceptual awareness , 2005, Neuropsychologia.

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

[113]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[114]  C. Frith,et al.  Self-awareness and action , 2003, Current Opinion in Neurobiology.

[115]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[116]  Karl J. Friston,et al.  The mirror-neuron system: a Bayesian perspective. , 2007, Neuroreport.

[117]  M. Goldberg,et al.  Single neurons in posterior cingulate cortex of behaving macaque: eye movement signals. , 1996, Journal of neurophysiology.

[118]  M Petrides,et al.  Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[120]  G. Gregoriou,et al.  The Intraparietal Cortex: Subregions Involved in Fixation, Saccades, and in the Visual and Somatosensory Guidance of Reaching , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[121]  F. Lacquaniti,et al.  Combination of hand and gaze signals during reaching: activity in parietal area 7 m of the monkey. , 1997, Journal of neurophysiology.

[122]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[123]  R. Hari,et al.  Modulated Activation of the Human SI and SII Cortices during Observation of Hand Actions , 2002, NeuroImage.