Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5

We traced the cortical connections of the anterior sector (F5a) of the macaque ventral premotor (PMv) area F5 and compared them with those of the adjacent F5 sectors, F5c and F5p. F5a displays a very dense “intrinsic” connectivity with F5c and F5p, premotor connections limited to F4 and F6/pre-SMA, relatively robust prefrontal connections with areas 46v and 12, and dense connections with rostral opercular frontal areas. Outside the frontal cortex, connections of F5a are dense with the SII region, relatively robust with inferior parietal areas PFG and AIP, weak with the inferior parietal area PF, and moderate with area 24. The comparison with data from injections in F5c and F5p showed that F5a, though sharing some common parietal connections with the other F5 sectors, displays several characterizing features providing robust evidence for its connectional distinctiveness. The present study provides evidence for a general organization of the PMv similar to that of the medial and dorsal premotor cortex, with F5a representing a pre-PMv area. Specifically, the present data suggest that F5a is a privileged site of integration, in the PMv, of parietal sensory-motor signals with higher-order information originating from prefrontal, rostral frontal opercular areas, and F6/pre-SMA. The results of this integration can be then broadcasted to the adjacent F5 sectors for the generation and control of hand actions and cognitive motor functions.

[1]  K. Akert,et al.  Insular and opercular cortex and its thalamic projection in Macaca mulatta. , 1963, Schweizer Archiv fur Neurologie, Neurochirurgie und Psychiatrie = Archives suisses de neurologie, neurochirurgie et de psychiatrie.

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

[3]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

[4]  H. Künzle An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. , 1978, Brain, behavior and evolution.

[5]  H Burton,et al.  Somatotopographic organization in the second somatosensory area of M. fascicularis , 1980, The Journal of comparative neurology.

[6]  G. Rizzolatti,et al.  Response properties and behavioral modulation of ‘mouth’ neurons of the postarcuate cortex (area 6) in macaque monkeys , 1981, Brain Research.

[7]  H. Kuypers,et al.  Fluorescent Neuronal Tracers , 1984 .

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

[9]  G. Rizzolatti,et al.  Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey , 1985, Behavioural Brain Research.

[10]  J. Tanji,et al.  Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[12]  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.

[13]  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.

[14]  F. Condé Further studies on the use of the fluorescent tracers fast blue and diamidino yellow: Effective uptake area and cellular storage sites , 1987, Journal of Neuroscience Methods.

[15]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[16]  B. Sessle,et al.  Input-output relationships of the primary face motor cortex in the monkey (Macaca fascicularis). , 1989, Journal of neurophysiology.

[17]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[18]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[19]  Kiyoshi Kurata,et al.  Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys , 1991, Neuroscience Research.

[20]  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.

[21]  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.

[22]  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.

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

[24]  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.

[25]  T. Deacon Cortical connections of the inferior arcuate sulcus cortex in the macaque brain , 1992, Brain Research.

[26]  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.

[27]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[28]  M. Hepp-Reymond,et al.  Force-related neuronal activity in two regions of the primate ventral premotor cortex. , 1994, Canadian journal of physiology and pharmacology.

[29]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[30]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[31]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  S. Ghosh,et al.  A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. , 1995, Somatosensory & motor research.

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

[34]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

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

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

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

[38]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[39]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[40]  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.

[41]  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.

[42]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.

[43]  K. Carlsson,et al.  Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus , 2000, Journal of Cognitive Neuroscience.

[44]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[45]  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.

[46]  G. Luppino,et al.  Interactive 3-D Reconstruction and Visualization of Primates Cerebral Cortex , 2001 .

[47]  G. Rizzolatti,et al.  I Know What You Are Doing A Neurophysiological Study , 2001, Neuron.

[48]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

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

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

[51]  Enrico Gobbetti,et al.  Three-dimensional Reconstruction and Visualization of the Cerebral Cortex in Primates , 2001, VisSym.

[52]  Yan Wang,et al.  Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex , 2002, Neuroreport.

[53]  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.

[54]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[55]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[56]  David J. Freedman,et al.  The prefrontal cortex: categories, concepts and cognition. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[57]  G. Luppino,et al.  ß Federation of European Neuroscience Societies Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey , 2022 .

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

[59]  R. Lemon,et al.  Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. , 2003, Journal of neurophysiology.

[60]  G. Rizzolatti,et al.  ß Federation of European Neuroscience Societies Mirror , 2003 .

[61]  R. Lemon,et al.  Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study , 2004, Experimental Brain Research.

[62]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[63]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

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

[65]  R. Lemon,et al.  Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. , 2004, The Journal of Neuroscience.

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

[67]  John W. Lane,et al.  Receptive Field Properties of the Macaque Second Somatosensory Cortex: Evidence for Multiple Functional Representations , 2004, The Journal of Neuroscience.

[68]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

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

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

[71]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[72]  G. Orban,et al.  Observing Others: Multiple Action Representation in the Frontal Lobe , 2005, Science.

[73]  M. Petrides,et al.  Orofacial somatomotor responses in the macaque monkey homologue of Broca's area , 2005, Nature.

[74]  J. Tanji,et al.  Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period. , 2005, Cerebral cortex.

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

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

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

[78]  M. Graziano The organization of behavioral repertoire in motor cortex. , 2006, Annual review of neuroscience.

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

[80]  Binary-Coded Monitoring of a Behavioral Sequence by Cells in the Pre-Supplementary Motor Area , 2006, The Journal of Neuroscience.

[81]  J. Tanji,et al.  Activity in the Lateral Prefrontal Cortex Reflects Multiple Steps of Future Events in Action Plans , 2006, Neuron.

[82]  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.

[83]  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.

[84]  G. Luppino,et al.  Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey , 2007, Brain Structure and Function.

[85]  J. Tanji,et al.  Role of the lateral prefrontal cortex in executive behavioral control. , 2008, Physiological reviews.

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

[87]  Marco Davare,et al.  Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans , 2008, The Journal of physiology.

[88]  Antonis P. Stylianou,et al.  An Additional Motor-Related Field in the Lateral Frontal Cortex of Squirrel Monkeys , 2008, Cerebral Cortex.

[89]  C. Acuña,et al.  Neural Correlates of Decisions and Their Outcomes in the Ventral Premotor Cortex , 2008, The Journal of Neuroscience.

[90]  G. Rizzolatti,et al.  Functional Organization of Inferior Parietal Lobule Convexity in the Macaque Monkey: Electrophysiological Characterization of Motor, Sensory and Mirror Responses and Their Correlation with Cytoarchitectonic Areas , 2022 .

[91]  Ranulfo Romo,et al.  Neural encoding of auditory discrimination in ventral premotor cortex , 2009, Proceedings of the National Academy of Sciences.

[92]  Guy A. Orban,et al.  The monkey ventral premotor cortex processes 3D shape from disparity , 2009, NeuroImage.

[93]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[94]  Marzio Gerbella,et al.  Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex , 2009, The Journal of comparative neurology.

[95]  Jose L Pardo-Vazquez,et al.  A role for the ventral premotor cortex beyond performance monitoring , 2009, Proceedings of the National Academy of Sciences.

[96]  Hideki Shimazu,et al.  Modulation of primary motor cortex outputs from ventral premotor cortex during visually guided grasp in the macaque monkey , 2009, The Journal of physiology.

[97]  Marzio Gerbella,et al.  Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord , 2010, The Journal of comparative neurology.

[98]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[99]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.