A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex.

The cortical connections of the dorsal (PMd) and ventral (PMv) subdivisions of the premotor area (PM, lateral area 6) were studied in four monkeys (Macaca fascicularis) through the use of retrograde tracers. In two animals, tracer was injected ventral to the arcuate sulcus (PMv), in a region from which forelimb movements could be elicited by intracortical microstimulation (ICMS). Tracer injections dorsal to the arcuate sulcus (PMd) were made in two locations. In one animal, tracer was injected caudal to the genu of the arcuate sulcus (in caudal PMd [cPMd], where ICMS was effective in eliciting forelimb movements); in another animal, it was injected rostral to the genu of the arcuate sulcus (in rostral PMd [rPMd], where ICMS was ineffective in eliciting movements). Retrogradely labeled neurons were counted in the ipsilateral hemisphere and located in cytoarchitectonically identified areas of the frontal and parietal lobes. Although both PMv and PMd were found to receive inputs from other motor areas, the prefrontal cortex, and the parietal cortex, there were differences in the topography and the relative strength of projections from these areas. There were few common inputs to PMv and PMd; only the supplementary eye fields projected to all three areas studied. Interconnections within PMd or PMv appeared to link hindlimb and forelimb representations, and forelimb and face representations; however, connections between PMd and PMv were sparse. Areas cPMd and PMv were found to receive inputs from other motor areas--the primary motor area, the supplementary motor area, and the cingulate motor area--but the topography and strength of projections from these areas varied. Area rPMd was found to receive sparse inputs, if any, from these motor areas. The frontal eye field (area 8a) was found to project to PMv and rPMd, and area 46 was labeled substantially only from rPMd. Parietal projections to PMv were found to originate from a variety of somatosensory and visual areas, including the second somatosensory cortex and related areas in the parietal operculum of the lateral sulcus, as well as areas 5, 7a, and 7b, and the anterior intraparietal area. By contrast, projections to cPMd arose only from area 5. Visual areas 7m and the medial intraparietal area were labeled from rPMd. Relatively more parietal neurons were labeled after tracer injections in PMv than in PMd. Thus, PMv and PMd appear to be parts of separate, parallel networks for movement control.

[1]  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.

[2]  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.

[3]  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.

[4]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

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

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

[7]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[8]  S. Wise,et al.  The premotor cortex of the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  J. Kaas,et al.  Supplementary eye field as defined by intracortical microstimulation: Connections in macaques , 1990, The Journal of comparative neurology.

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

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

[12]  K. Kurata,et al.  Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movements. , 1993, Journal of neurophysiology.

[13]  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.

[14]  Hiroshi Asanuma,et al.  Noxious effects of excessive currents used for intracortical microstimulation , 1975, Brain Research.

[15]  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.

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

[17]  G. V. Van Hoesen,et al.  Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey , 1993, The Journal of comparative neurology.

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

[19]  C. Brinkman,et al.  Supplementary motor area in the monkey: activity of neurons during performance of a learned motor task. , 1979, Journal of neurophysiology.

[20]  C. Darian‐Smith,et al.  Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey , 1993, The Journal of comparative neurology.

[21]  P. Strick,et al.  Medial wall motor areas and skeletomotor control , 1992, Current Opinion in Neurobiology.

[22]  Richard A. Andersen,et al.  Coordinate transformations in the representation of spatial information , 1993, Current Opinion in Neurobiology.

[23]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses , 1981, Behavioural Brain Research.

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

[25]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

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

[27]  D. Hoffman,et al.  Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. , 1994, Journal of neurophysiology.

[28]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[29]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[30]  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.

[31]  M. Wiesendanger,et al.  Structural and functional definition of the motor cortex in the monkey (Macaca fascicularis) , 1982, The Journal of physiology.

[32]  M. Mesulam,et al.  Tracing Neural Connections with Horseradish Peroxidase , 1982 .

[33]  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.

[34]  K. Noguchi,et al.  Gene regulation in an ascending nociceptive pathway: inflammation- induced increase in preprotachykinin mRNA in rat lamina I spinal projection neurons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  J Tanji,et al.  Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their relation to a trained motor task. , 1994, Journal of neurophysiology.

[36]  S. Bisti,et al.  Light sensitivity, adaptation and saturation in mammalian rods. , 1993, Progress in brain research.

[37]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

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

[39]  I. Darian‐Smith,et al.  Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. , 1994, Cerebral cortex.

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

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

[42]  K. Toyoshima,et al.  Exact cortical extent of the origin of the corticospinal tract (CST) and the quantitative contribution to the CST in different cytoarchitectonic areas. A study with horseradish peroxidase in the monkey. , 1982, Journal fur Hirnforschung.

[43]  K Watanabe,et al.  Connections of area 8 with area 6 in the brain of the macaque monkey , 1988, The Journal of comparative neurology.

[44]  K. Kubota,et al.  Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas) , 1991, The Journal of comparative neurology.

[45]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[46]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. , 1985, Journal of neurophysiology.

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

[48]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

[49]  R Porter,et al.  Supplementary motor area and premotor area of monkey cerebral cortex: functional organization and activities of single neurons during performance of a learned movement. , 1983, Advances in neurology.

[50]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

[51]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[53]  E. G. Jones,et al.  Possible determinants of the degree of retrograde neuronal labeling with horseradish peroxidase , 1975, Brain Research.

[54]  K. Kurata Information processing for motor control in primate premotor cortex , 1994, Behavioural Brain Research.

[55]  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.

[56]  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.

[57]  R Porter,et al.  Morphology of pyramidal neurones in monkey motor cortex and the synaptic actions of their intracortical axon collaterals. , 1988, The Journal of physiology.

[58]  P S Goldman-Rakic,et al.  Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

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

[60]  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.

[61]  S P Wise,et al.  A neurophysiological comparison of three distinct regions of the primate frontal lobe. , 1991, Brain : a journal of neurology.

[62]  S. Wise,et al.  A neurophysiological study of the premotor cortex in the rhesus monkey. , 1984, Brain : a journal of neurology.

[63]  D. Johnston,et al.  Rectification of single GABA-gated chloride channels in adult hippocampal neurons. , 1985, Journal of neurophysiology.

[64]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[65]  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.

[66]  Harold Burton,et al.  Second Somatosensory Cortex and Related Areas , 1986 .

[67]  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.

[68]  M. Schlag-Rey,et al.  Evidence for a supplementary eye field. , 1987, Journal of neurophysiology.

[69]  J Tanji,et al.  Comparison of movement-related activity in two cortical motor areas of primates. , 1982, Journal of neurophysiology.

[70]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses , 1981, Behavioural Brain Research.

[71]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[72]  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.

[73]  R. Lemon,et al.  The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements , 1985, Behavioural Brain Research.

[74]  D. Pandya,et al.  Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. , 1971, Brain research.