Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action.

The cortical projections to the caudal part of the superior parietal lobule (area PEc) were studied in 6 cynomolgus monkeys using fluorescence tracers. Significant numbers of labeled cells were found in a restricted network of parietal, mesial, and frontal areas. Quantitative analysis demonstrated that approximately 30% of the total projection neurons originated in the adjacent areas of the dorsocaudal part of the superior parietal lobule (areas PE and V6A). The medial bank of the intraparietal sulcus, inferior parietal lobule, and frontal lobe (mainly the dorsocaudal part of premotor area F2) each contributed approximately 15% of the projection neurons. About 15% of the labeled neurons were located in the posterior cingulate area (PEci) and another 10% in other areas of the mesial surface of the hemisphere. Based on these data, we suggest that PEc processes information about the position of the limbs. The specific anatomical links between PEc and motor and premotor areas that host a representation of the lower limbs, together with the link with vestibular cortex and with areas involved in the analysis of optic flow and spatial navigation, imply a role for PEc in locomotion and coordinated limb movement in the environment.

[1]  Robert Desimone,et al.  Cortical Connections of Area V4 in the Macaque , 2008 .

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

[3]  O. Grüsser,et al.  Responses of Single Neurons in the Parietoinsular Vestibular Cortex of Primates a , 1988, Annals of the New York Academy of Sciences.

[4]  Mario Fiorani,et al.  Parallel Evolution of Cortical Areas Involved in Skilled Hand Use , 2007, The Journal of Neuroscience.

[5]  J. Hyvärinen.  Posterior parietal lobe of the primate brain. , 1982, Physiological reviews.

[6]  F. Duffy,et al.  Somatosensory System: Organizational Hierarchy from Single Units in Monkey Area 5 , 1971, Science.

[7]  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.

[8]  H. Ku¨nzle,et al.  Cortico-cortical efferents of primary motor and somatosensory regions of the cerebral cortex in Macaca fascicularis , 1978, Neuroscience.

[9]  M. Wiesendanger,et al.  Sensory inputs to the agranular motor fields: a comparison between precentral, supplementary-motor and premotor areas in the monkey , 2004, Experimental Brain Research.

[10]  G. Luppino,et al.  Visual responses in the dorsal premotor area F2 of the macaque monkey , 1999, Experimental Brain Research.

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

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

[13]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Claus C Hilgetag,et al.  Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex , 2005, The European journal of neuroscience.

[15]  Mark W Greenlee,et al.  Neural correlates of visually induced self-motion illusion in depth. , 2008, Cerebral cortex.

[16]  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.

[17]  J. Tanji,et al.  A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. , 1992, Journal of neurophysiology.

[18]  Guldin Wo,et al.  Is there a vestibular cortex , 1998 .

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

[20]  K. Brodmann.  Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[21]  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.

[22]  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.

[23]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[24]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

[25]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[26]  S P Wise,et al.  The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  A. Battaglia-Mayer,et al.  Visual Motion Responses of Neurons in the Caudal Area PE of Macaque Monkeys , 2001, The Journal of Neuroscience.

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

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

[30]  J. Lynch.  The functional organization of posterior parietal association cortex , 1980, Behavioral and Brain Sciences.

[31]  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.

[32]  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.

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

[34]  T. Peele.  Cytoarchitecture of individual parietal areas in the monkey (Macaca mulatta) and the distribution of the efferent fibers , 1942 .

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

[36]  P. Strick,et al.  Corticospinal projections from the medial wall of the hemisphere , 2004, Experimental Brain Research.

[37]  Elisabeth A. Murray,et al.  Supplementary Sensory Area , 1981 .

[38]  Milena Raffi,et al.  Neuronal responses to optic flow in the monkey parietal area PEc. , 2002, Cerebral cortex.

[39]  E. Jankowska,et al.  Projections of pyramidal tract cells to alpha‐motoneurones innervating hind‐limb muscles in the monkey. , 1975, The Journal of physiology.

[40]  B. Vogt,et al.  Architecture and neurocytology of monkey cingulate gyrus , 2005, The Journal of comparative neurology.

[41]  C. Galletti,et al.  Arm Movement‐related Neurons in the Visual Area V6A of the Macaque Superior Parietal Lobule , 1997, The European journal of neuroscience.

[42]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  Marzio Gerbella,et al.  A multiarchitectonic approach for the definition of functionally distinct areas and domains in the monkey frontal lobe , 2007, Journal of anatomy.

[44]  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.

[45]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[46]  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.

[47]  A. Wunderlich,et al.  Brain activation during human navigation: gender-different neural networks as substrate of performance , 2000, Nature Neuroscience.

[48]  G. Leichnetz.  Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[49]  P. Strick,et al.  Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas , 1979, Brain Research.

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

[51]  Claudio Galletti,et al.  Functional imaging of the parietal cortex during action execution and observation. , 2009, Cerebral cortex.

[52]  Simona Monaco,et al.  Visual, somatosensory, and bimodal activities in the macaque parietal area PEc. , 2008, Cerebral cortex.

[53]  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.

[54]  G. Rizzolatti,et al.  Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey , 1991, The Journal of comparative neurology.

[55]  Michela Gamberini,et al.  Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas , 2006, The Journal of comparative neurology.

[56]  S P Wise,et al.  Submodality distribution in sensorimotor cortex of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[57]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[58]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[59]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[60]  Deepak N. Pandya,et al.  Further observations on corticofrontal connections in the rhesus monkey , 1976, Brain Research.

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

[62]  M. Gamberini,et al.  Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[63]  K. Kurata,et al.  Distribution of neurons with set- and movement-related activity before hand and foot movements in the premotor cortex of rhesus monkeys , 2004, Experimental Brain Research.

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

[65]  C. Galletti,et al.  The relationship between V6 and PO in macaque extrastriate cortex , 2005, The European journal of neuroscience.

[66]  O. Grüsser,et al.  Is there a vestibular cortex? , 1998, Trends in Neurosciences.

[67]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

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

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

[70]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[71]  Atsushi Nambu,et al.  Somatotopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortex in the macaque monkey , 2001, Neuroscience Research.

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

[73]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[75]  Lauretta Passarelli,et al.  Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey , 2009, The Journal of comparative neurology.

[76]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[77]  C. Galletti,et al.  Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex , 2009, The Journal of Neuroscience.

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

[79]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[80]  D. Boussaoud,et al.  Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways , 2002, Experimental Brain Research.

[81]  R Caminiti,et al.  Early coding of visuomanual coordination during reaching in parietal area PEc. , 2001, Journal of neurophysiology.

[82]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

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

[84]  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.

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

[86]  Elisabeth A. Murray,et al.  Supplementary Sensory Area The Medial Parietal Cortex in the Monkey , 1981 .

[87]  Giorgio M Innocenti,et al.  Areal organization of the posterior parietal cortex of the ferret (Mustela putorius). , 2002, Cerebral cortex.

[88]  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.

[89]  Andrew T. Smith,et al.  The Representation of Egomotion in the Human Brain , 2008, Current Biology.

[90]  Hideo Sakata,et al.  Navigation-associated medial parietal neurons in monkeys , 2006, Proceedings of the National Academy of Sciences.

[91]  Atsushi Iriki,et al.  Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys , 2000, Experimental Brain Research.

[92]  Matthew W Spitzer,et al.  Anatomical and physiological definition of the motor cortex of the marmoset monkey , 2008, The Journal of comparative neurology.

[93]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[94]  G. Rizzolatti,et al.  Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: An intracortical microstimulation study in the macaque monkey , 1991, The Journal of comparative neurology.

[95]  R Caminiti,et al.  Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. , 2001, Cerebral cortex.

[96]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[97]  Andrew R Mitz,et al.  Somatotopy of monkey premotor cortex examined with microstimulation , 1995, Neuroscience Research.

[98]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[99]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[100]  A. Ballabeni,et al.  Neuronal responses in macaque area PEc to saccades and eye position , 2008, Neuroscience.

[101]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

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

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

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

[105]  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.