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01-03-2011 | Original Article

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

Authors: Marzio Gerbella, Abdelouahed Belmalih, Elena Borra, Stefano Rozzi, Giuseppe Luppino

Published in: Brain Structure and Function | Issue 1/2011

Abstract

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.

Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342CrossRefPubMed

Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256:211–228CrossRefPubMed

Belmalih A, Borra E, Contini M, Gerbella M, Rozzi S, Luppino G (2007a) A multiarchitectonic approach for the definition of functionally distinct areas and domains in the monkey frontal lobe. J Anat 211:199–211CrossRefPubMed

Belmalih A, Borra E, Gerbella M, Rozzi S, Luppino G (2007b) Connections of architectonically distinct subdivisions of the ventral premotor area F5 of the macaque. Program No 6365 2007 Neuroscience Meeting Planner. Society for Neuroscience, San Diego, CA, 2007 Online

Belmalih A, Borra E, Contini M, Gerbella M, Rozzi S, Luppino G (2009) Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. J Comp Neurol 512:183–217CrossRefPubMed

Bettio F, Demelio S, Gobbetti E, Luppino G, Matelli M (2001) Interactive 3-D reconstruction and visualization of primates cerebral cortex. Society for Neuroscience Abstracts:728.724

Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund HJ (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11:3276–3286CrossRefPubMed

Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A, Rozzi S, Luppino G (2008) Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb Cortex 18:1094–1111CrossRefPubMed

Borra E, Belmalih A, Gerbella M, Rozzi S, Luppino G (2010) Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord. J Comp Neurol 518:2570–2591PubMed

Carlsson K, Petrovic P, Skare S, Petersso KM, Ingvar M (2000) Tickling expectations: neural processing in anticipation of a sensory stimulus. J Cogn Neurosci 12:691–703CrossRefPubMed

Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402CrossRefPubMed

Carmichael ST, Price JL (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664CrossRefPubMed

Cerri G, Shimazu H, Maier MA, Lemon RN (2003) Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. J Neurophysiol 90:832–842CrossRefPubMed

Cipolloni PB, Pandya DN (1999) Cortical connections of the frontoparietal opercular areas in the rhesus monkey. J Comp Neurol 403:431–458CrossRefPubMed

Condé F (1987) Further studies on the use of the fluorescent tracers fast blue and diamidino yellow: effective uptake area and cellular storage sites. J Neurosci Meth 21:31–43CrossRef

Dancause N, Duric V, Barbay S, Frost SB, Stylianou A, Nudo RJ (2008) An additional motor-related field in the lateral frontal cortex of squirrel monkeys. Cereb Cortex 18:2719–2728CrossRefPubMed

Davare M, Andres M, Cosnard G, Thonnard J-L, Olivier E (2006) Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J Neurosci 26:2260–2268CrossRefPubMed

Davare M, Lemon R, Olivier E (2008) Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J Physiol 586:2735–2742CrossRefPubMed

Deacon TW (1992) Cortical connections of the inferior arcuate sulcus cortex in the macaque brain. Brain Res 573:8–26CrossRefPubMed

Demelio S, Bettio F, Gobbetti E, Luppino G (2001) Three-dimensional reconstruction and visualization of the cerebral cortex in primates. In: Ebert D, Favre J, Peikert R (eds) Data visualization 2001. Proceedings of the Joint Eurographics and IEEE TCGV Symposium on visualization, Ascona, Switzerland, May 28–30, 2001

Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667–689PubMed

Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77:677–682CrossRefPubMed

Dum RP, Strick PL (2005) Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci 25:1375–1386CrossRefPubMed

Ehrsson HH, Fagergren A, Forssberg H (2001) Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. J Neurophysiol 85:2613–2623PubMed

Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in primate cerebral cortex. Cereb Cor 1:1–47CrossRef

Ferrari PF, Gallese V, Rizzolatti G, Fogassi L (2003) Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17:1703–1714CrossRefPubMed

Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS (2004) Receptive field properties of the macaque second somatosensory cortex: evidence for multiple functional representations. J Neurosci 24:11193–11204CrossRefPubMed

Fogassi L, Luppino G (2005) Motor functions of the parietal lobe. Curr Opin Neurobiol 15:626–631CrossRefPubMed

Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667CrossRefPubMed

Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609CrossRefPubMed

Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey: I. Somatotopy and the control of proximal movements. Exp Brain Res 71:475–490CrossRefPubMed

Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2007) Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey. Brain Struct Funct 212:269–301CrossRefPubMed

Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2010) Cortical connections of the macaque caudal ventrolateral prefrontal areas 45a and 45b. Cereb Cortex 20:141–168CrossRefPubMed

Ghosh S, Gattera R (1995) A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. Somat Mot Res 12:359–378CrossRef

Godschalk M, Lemon RN, Kuypers HGJM, Ronday HK (1984) Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res 56:410–424CrossRefPubMed

Graziano M (2006) The organization of behavioral repertoire in motor cortex. Ann Rev Neurosci 29:105–134CrossRefPubMed

Gregoriou GG, Borra E, Matelli M, Luppino G (2006) Architectonic organization of the inferior parietal convexity of the macaque monkey. J Comp Neurol 496:422–451CrossRefPubMed

Grezes J, Armony JL, Rowe J, Passingham RE (2003) Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study. NeuroImage 18:928–937CrossRefPubMed

Hepp-Reymond M-C, Hüsler EJ, Maier MA, Qi H-X (1994) Force-related neuronal activity in two regions of the primate ventral premotor cortex. Can J Physiol Pharmacol 72:571–579PubMed

Huang CS, Hiraba H, Sessle BJ (1989) Input-output relationships of the primary face motor cortex in the monkey (macaca fascicularis). J Neurophysiol 61:350–362PubMed

Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320CrossRefPubMed

Joly O, Vanduffel W, Orban GA (2009) The monkey ventral premotor cortex processes 3D shape from disparity. NeuroImage 47:262–272CrossRefPubMed

Jones EG, Burton H (1976) Areal differences in the laminar distribution of thalamic afferences in cortical fields of the insular, parietal and temporal regions of primates. J Comp Neurol 168:197–248CrossRefPubMed

Kohler E, Keysers C, Umilta MA, Fogassi L, Gallese V, Rizzolatti G (2002) Hearing sounds, understanding actions: action representation in mirror neurons. Science 297:846–848CrossRefPubMed

Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M (1995) A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci 15:3821–3839PubMed

Kunzle H (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (area 6 and 9) in Macaca fascicularis. Brain Behav Evol 15:185–234CrossRefPubMed

Kurata K (1991) Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys. Neurosci Res 12:263–280CrossRefPubMed

Kurata K, Tanji J (1986) Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci 6:403–411PubMed

Kuypers HGJM, Huisman AM (1984) Fluorescent neuronal tracers. Adv Cell Neurobiol 5:307–340

Lemus L, Hernandez A, Romo R (2009) Neural encoding of auditory discrimination in ventral premotor cortex. Proc Natl Acad Sci USA 106:14640–14645CrossRefPubMed

Levy R, Goldman Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32CrossRefPubMed

Lu MT, Preston JB, Strick PL (1994) Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J Comp Neurol 341:375–392CrossRefPubMed

Luppino G, Matelli M, Camarda R, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study. J Comp Neurol 311:463–482CrossRefPubMed

Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area f3 (SMA-proper) and area f6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140CrossRefPubMed

Luppino G, Murata A, Govoni P, Matelli M (1999) Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4). Exp Brain Res 128:181–187CrossRefPubMed

Luppino G, Rozzi S, Calzavara R, Matelli M (2003) Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur J Neurosci 17:559–578CrossRefPubMed

Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of macaque monkey. Behav Brain Res 18:125–137CrossRefPubMed

Matelli M, Camarda R, Glickstein M, Rizzolatti G (1986) Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251:281–298CrossRefPubMed

Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and of the adjacent cingulate cortex. J Comp Neurol 311:445–462CrossRefPubMed

Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G (1998) Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402:327–352CrossRefPubMed

Matelli M, Luppino G, Geyer S, Zilles K (2004) Motor cortex. In: Paxinos G, Mai JK (eds) The human nervous system, 2nd edn. Elsevier, San Diego, pp 975–996

Matsuzaka Y, Aizawa H, Tanji J (1992) A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol 68:653–662PubMed

Miller EK, Freedman DJ, Wallis JD (2002) The prefrontal cortex: categories, concepts and cognition. Phil Trans R Soc B 357:1123CrossRefPubMed

Mitz AR, Wise SP (1987) The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping. J Neurosci 7:1010–1021PubMed

Murata A, Gallese V, Luppino G, Kaseda M, Sakata H (2000) Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J Neurophysiol 83:2580–2601PubMed

Mushiake H, Saito N, Sakamoto K, Itoyama Y, Tanji J (2006) Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans. Neuron 50:631CrossRefPubMed

Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing others: multiple action representation in the frontal lobe. Science 310:332–336CrossRefPubMed

Pandya DN, Kuypers HGJM (1969) Cortico-cortical connections in the rhesus monkey. Brain Res 13:13–36CrossRefPubMed

Pardo-Vazquez JL, Leboran V, Acuna C (2008) Neural correlates of decisions and their outcomes in the ventral premotor cortex. J Neurosci 28:12396–12408CrossRefPubMed

Pardo-Vazquez JL, Leboran V, Acuna C (2009) A role for the ventral premotor cortex beyond performance monitoring. Proc Natl Acad Sci USA 106:18815–18819CrossRefPubMed

Passingham RE, Toni I, Rushworth MFS (2000) Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning. Exp Brain Res 133:103–113CrossRefPubMed

Petrides M, Cadoret G, Mackey S (2005) Orofacial somatomotor responses in the macaque monkey homologue of Broca’s area. Nature 435:1235CrossRefPubMed

Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11:663–672CrossRefPubMed

Pons T, Garraghty P, Cusick C, Kaas J (1985) The somatotopic organization of area 2 in macaque monkeys. J Comp Neurol 241:445–466CrossRefPubMed

Prabhu G, Shimazu H, Cerri G, Brochier T, Spinks RL, Maier MA, Lemon RN (2009) Modulation of primary motor cortex outputs from ventral premotor cortex during visually guided grasp in the macaque monkey. J Physiol 587:1057–1069CrossRefPubMed

Preuss TM, Goldman-Rakic PS (1989) 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. J Comp Neurol 282:293–316CrossRefPubMed

Raos V, Umilta M-A, Murata A, Fogassi L, Gallese V (2006) Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J Neurophysiol 95:709–729CrossRefPubMed

Rathelot J-A, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci USA 106(3):918–923CrossRefPubMed

Rizzolatti G, Craighero L (2004) The mirror neuron system. Ann Rev Neurosci 27:169–192CrossRefPubMed

Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901CrossRefPubMed

Rizzolatti G, Sinigaglia C (2010) The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 11:264CrossRefPubMed

Rizzolatti G, Scandolara C, Gentilucci M, Camarda R (1981) Response properties and behavioural modulation of “mouth” neurons of the postarcuate cortex (area 6) in macaque monkey. Brain Res 255:421–424CrossRef

Rizzolatti G, Camarda R, Fogassi M, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey: II. Area F5 and the control of distal movements. Exp Brain Res 71:491–507CrossRefPubMed

Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Cogn Brain Res 3:131–141CrossRef

Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296CrossRefPubMed

Roberts T, Akert K (1963) Insular and opercular cortex and its thalamic projections in Macaca mulatta. Sweiz Archiv Neurol Neurochir Psychiatr 92:1–43

Robinson CJ, Burton H (1980) Somatotopographic organization in the second somatosensory area of M. fascicularis. J Comp Neurol 192:43–67CrossRefPubMed

Romo R, Hernández A, Zainos A (2004) Neuronal correlates of a perceptual decision in ventral premotor cortex. Neuron 41:165CrossRefPubMed

Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16:1389–1417CrossRefPubMed

Rozzi S, Ferrari P, Bonini L, Rizzolatti G, Fogassi L (2008) 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. Eur J Neurosci 28:1569–1588CrossRefPubMed

Saito N, Mushiake H, Sakamoto K, Itoyama Y, Tanji J (2005) Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period. Cereb Cortex 15:1535–1546CrossRefPubMed

Shima K, Tanji J (2006) Binary-coded monitoring of a behavioral sequence by cells in the pre-supplementary motor area. J Neurosci 26:2579–2582CrossRefPubMed

Shimazu H, Maier MA, Cerri G, Kirkwood PA, Lemon RN (2004) Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J Neurosci 24:1200–1211CrossRefPubMed

Taira M, Mine S, Georgopulos AP, Murata A, Sakata H (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res 83:29–36CrossRefPubMed

Tanji J, Hoshi E (2008) Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88:37–57CrossRefPubMed

Tanne Gariepy J, Rouiller EM, Boussaoud D (2002) Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91–103CrossRefPubMed

Umilta MA, Kohler E, Gallese V, Fogassi L, Fadiga L, Keysers C, Rizzolatti G (2001) I know what you are doing: a neurophysiological study. Neuron 31:155–165CrossRefPubMed

Umilta MA, Brochier T, Spinks RL, Lemon RN (2007) Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. J Neurophysiol 98:488–501CrossRefPubMed

Wang Y, Shima K, Isoda M, Sawamura H, Tanji J (2002) Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex. Neuroreport 13:1341–1344CrossRefPubMed

Webster MJ, Bachevalier J, Ungerleider LG (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 4:470–483CrossRefPubMed

Title: Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5
Authors: Marzio Gerbella
Abdelouahed Belmalih
Elena Borra
Stefano Rozzi
Giuseppe Luppino
Publication date: 01-03-2011
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 1/2011
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-010-0293-6

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

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