Progress in Motor Control pp 61-86 | Cite as
Plasticity in the Motor Network Following Primary Motor Cortex Lesion
Abstract
The behavioral deficits following stroke are particularly evident in the fine control of force, movement, and posture of the arm and hand. However, functional recovery continues in the weeks and months after the initial lesion. Various animal models of stroke have been used to investigate the mechanisms involved with this recovery. These studies have revealed a dramatic physiological and structural reorganization not only within the tissue surrounding the lesion but also in other distant areas of the brain in both the contralesional and ipsilesional hemispheres. These latter changes suggest that functional recovery could be dependent upon the adaptive plasticity of intact, remaining brain structures, a phenomenon often referred to as “vicariation of function”. In the case of a lesion in the primary motor cortex (M1), the premotor areas are particularly well positioned to substitute for the lost M1 function because of their extensive interconnections with other motor areas, their corticospinal outputs, and the movement-related activity they carry prior to the lesion. In the present chapter, the basic principles of organization of the primary motor and premotor cortex are reviewed with the addition of a few key studies carried out in monkeys that have contributed to our understandings of adaptive plasticity in the ipsilesional hemisphere after stroke.
Keywords
Squirrel Monkey Supplementary Motor Area Ventral Horn Premotor Area Rostral PortionNotes
Acknowledgments
The author wishes to extend grateful thanks to Dr. Kelsey D. Dancause for grammar and insightful editing and Dr. Allan Smith for suggestions on scientific content. Numa Dancause is currently holding a Chercheur Boursier Junior 1 salary award from the Fonds de la Recherche en Santé du Québec (FRSQ) and a New Investigator salary award from the Canadian Institutes of Health Research (CIHR).
References
- Aizawa H, Inase M, Mushiake H, Shima K, Tanji J (1991) Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery. Exp Brain Res 84(3):668–671PubMedCrossRefGoogle Scholar
- Alexander GE, Crutcher MD (1990) Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol 64(1):133–150PubMedGoogle Scholar
- Alstermark B, Kummel H, Pinter MJ, Tantisira B (1990) Integration in descending motor pathways controlling the forelimb in the cat. 17. Axonal projection and termination of C3-C4 propriospinal neurones in the C6-Th1 segments. Exp Brain Res 81(3):447–461PubMedCrossRefGoogle Scholar
- Asanuma H, Pavlides C (1997) Neurobiological basis of motor learning in mammals. Neuroreport 8(4):i–viPubMedCrossRefGoogle Scholar
- Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256(2):211–228PubMedCrossRefGoogle Scholar
- Bates JF, Goldman-Rakic PS (1993) Prefrontal connections of medial motor areas in the rhesus monkey. J Comp Neurol 336(2):211–228PubMedCrossRefGoogle Scholar
- Bennett KM, Lemon RN (1996) Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. J Neurophysiol 75(5):1826–1842PubMedGoogle Scholar
- Bortoff GA, Strick PL (1993) Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J Neurosci 13(12):5105–5118PubMedGoogle Scholar
- Boudrias M-H, Cheney PD (2006) Output properties of premotor ventral area (PMv) in rhesus macaques. Paper presented at the society for the neural control of movement, 16th annual meeting, Key Biscayne, FLGoogle Scholar
- Brinkman C (1984) Supplementary motor area of the monkey’s cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4(4):918–929PubMedGoogle Scholar
- Buys EJ, Lemon RN, Mantel GW, Muir RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J Physiol 381:529–549PubMedGoogle Scholar
- Carey LM, Abbott DF, Egan GF, Bernhardt J, Donnan GA (2005) Motor impairment and recovery in the upper limb after stroke. Behavioral and neuroanatomical correlates. Stroke 36:625–629PubMedCrossRefGoogle Scholar
- Carey LM, Abbott DF, Egan GF, O’Keefe GJ, Jackson GD, Bernhardt J et al (2006) Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil Neural Repair 20(1):24–41PubMedCrossRefGoogle Scholar
- Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, Li S (2005) Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 193(2):291–311PubMedCrossRefGoogle Scholar
- 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(2):832–842PubMedCrossRefGoogle Scholar
- Cheney PD, Fetz EE (1985) Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. J Neurophysiol 53(3):786–804PubMedGoogle Scholar
- Crammond DJ, Kalaska JF (1994) Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J Neurophysiol 71(3):1281–1284PubMedGoogle Scholar
- Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV et al (2005) Extensive cortical rewiring after brain injury. J Neurosci 25(44):10167–10179PubMedCrossRefGoogle Scholar
- Dancause N, Barbay S, Frost SB, Plautz EJ, Popescu M, Dixon PM et al (2006a) Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cereb Cortex 16(8):1057–1068CrossRefGoogle Scholar
- Dancause N, Barbay S, Frost SB, Plautz EJ, Stowe AM, Friel KM et al (2006b) Ipsilateral connections of the ventral premotor cortex in a new world primate. J Comp Neurol 495(4):374–390CrossRefGoogle Scholar
- Dancause N, Barbay S, Frost SB, Zoubina EV, Plautz EJ, Mahnken JD et al (2006c) Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. J Neurophysiol 96(6):3506–3511CrossRefGoogle Scholar
- Dancause N, Barbay S, Frost SB, Mahnken JD, Nudo RJ (2007) Interhemispheric connections of the ventral premotor cortex in a new world primate. J Comp Neurol 505(6):701–715PubMedCrossRefGoogle Scholar
- 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(12):2719–2728PubMedCrossRefGoogle Scholar
- 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(Pt 11):2735–2742PubMedCrossRefGoogle Scholar
- Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11(3):667–689PubMedGoogle Scholar
- Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77(4–5):677–682PubMedCrossRefGoogle Scholar
- 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(6):1375–1386PubMedCrossRefGoogle Scholar
- Ebner TJ, Hendrix CM, Pasalar S (2009) Past, present, and emerging principles in the neural encoding of movement. Adv Exp Med Biol 629:127–137PubMedCrossRefGoogle Scholar
- Eisner-Janowicz I, Barbay S, Hoover E, Stowe AM, Frost SB, Plautz EJ et al (2008) Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. J Neurophysiol 100(3):1498–1512PubMedCrossRefGoogle Scholar
- Fang PC, Stepniewska I, Kaas JH (2005) Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti. J Comp Neurol 490(3):305–333PubMedCrossRefGoogle Scholar
- Fetz EE, Cheney PD (1980) Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44(4):751–772PubMedGoogle Scholar
- Fetz EE, Cheney PD, German DC (1976) Corticomotoneuronal connections of precentral cells detected by postspike averages of EMG activity in behaving monkeys. Brain Res 114(3):505–510PubMedCrossRefGoogle Scholar
- Florence SL, Taub HB, Kaas JH (1998) Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282(5391):1117–1121PubMedCrossRefGoogle Scholar
- Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G (2001) Cortical mechanism for the visual guidance of hand grasping movements in the monkey: a reversible inactivation study. Brain 124(Pt 3):571–586PubMedCrossRefGoogle Scholar
- Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG (2004) Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127(Pt 4):747–758PubMedCrossRefGoogle Scholar
- Friel KM, Barbay S, Frost SB, Plautz EJ, Hutchinson DM, Stowe AM et al (2005) Dissociation of sensorimotor deficits after rostral versus caudal lesions in the primary motor cortex hand representation. J Neurophysiol 94(2):1312–1324PubMedCrossRefGoogle Scholar
- Friel KM, Barbay S, Frost SB, Plautz EJ, Stowe AM, Dancause N et al (2007) Effects of a rostral motor cortex lesion on primary motor cortex hand representation topography in primates. Neurorehabil Neural Repair 21(1):51–61PubMedCrossRefGoogle Scholar
- Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ (2003) Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J Neurophysiol 89(6):3205–3214PubMedCrossRefGoogle Scholar
- Fulton J (1935) A note on the definition of the “motor” and “premotor” areas. Brain 58:311–316CrossRefGoogle Scholar
- 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(3):475–490PubMedCrossRefGoogle Scholar
- Georgopoulos AP, Stefanis CN (2007) Local shaping of function in the motor cortex: motor contrast, directional tuning. Brain Res Rev 55(2):383–389PubMedCrossRefGoogle Scholar
- Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2011). Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct Funct 216(1):43–65PubMedCrossRefGoogle Scholar
- Geyer S, Matelli M, Luppino G, Zilles K (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol (Berl) 202(6):443–474CrossRefGoogle Scholar
- Ghosh S, Gattera R (1995) A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. Somatosens Mot Res 12(3–4):359–378PubMedCrossRefGoogle Scholar
- Glees P, Cole J (1950) Recovery of skilled motor functions after small repeated lesions of motor cortex in macaque. J Neurophysiol 13:137–148Google Scholar
- Griffin DM, Hudson HM, Belhaj-Saif A, Cheney PD (2009) Stability of output effects from motor cortex to forelimb muscles in primates. J Neurosci 29(6):1915–1927PubMedCrossRefGoogle Scholar
- He SQ, Dum RP, Strick PL (1993) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci 13(3):952–980PubMedGoogle Scholar
- He SQ, Dum RP, Strick PL (1995) Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15(5 Pt 1):3284–3306PubMedGoogle Scholar
- Hepp-Reymond MC, Husler EJ, Maier MA, Ql HX (1994) Force-related neuronal activity in two regions of the primate ventral premotor cortex. Can J Physiol Pharmacol 72(5):571–579PubMedCrossRefGoogle Scholar
- Huntley GW, Jones EG (1991) Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. J Neurophysiol 66(2):390–413PubMedGoogle Scholar
- Kaas JH (1993) The functional organization of somatosensory cortex in primates. Anat Anz 175(6):509–518CrossRefGoogle Scholar
- Kalaska JF (2009) From intention to action: motor cortex and the control of reaching movements. Adv Exp Med Biol 629:139–178PubMedCrossRefGoogle Scholar
- Kalaska JF, Sergio LE, Cisek P (1998) Cortical control of whole-arm motor tasks. Novartis Found Symp 218:176–190; discussion 190–201PubMedGoogle Scholar
- Kermadi I, Liu Y, Tempini A, Rouiller EM (1997) Effects of reversible inactivation of the supplementary motor area (SMA) on unimanual grasp and bimanual pull and grasp performance in monkeys. Somatosens Mot Res 14(4):268–280PubMedCrossRefGoogle Scholar
- Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24(3):628–633PubMedCrossRefGoogle Scholar
- Kubota K (1996) Motor cortical muscimol injection disrupts forelimb movement in freely moving monkeys. Neuroreport 7(14):2379–2384PubMedCrossRefGoogle Scholar
- Kurata K, Hoffman DS (1994) Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. J Neurophysiol 71(3):1151–1164PubMedGoogle Scholar
- Kurata K, Wise SP (1988) Premotor and supplementary motor cortex in rhesus monkeys: neuronal activity during externally- and internally-instructed motor tasks. Exp Brain Res 72(2):237–248PubMedCrossRefGoogle Scholar
- Lai SM, Studenski S, Duncan PW, Perera S (2002) Persisting consequences of stroke measured by the Stroke Impact Scale. Stroke 33(7):1840–1844PubMedCrossRefGoogle Scholar
- Lashley KS (1929) Brain mechanisms and intelligence: a quantitative study of injuries to the brain. Chicago Press, ChicagoCrossRefGoogle Scholar
- Lashley KS (1930) Basic neural mechanisms in behavior. Psychol Rev 37:1–24CrossRefGoogle Scholar
- Lemon RN, Muir RB, Mantel GW (1987) The effects upon the activity of hand and forearm muscles of intracortical stimulation in the vicinity of corticomotor neurones in the conscious monkey. Exp Brain Res 66(3):621–637PubMedCrossRefGoogle Scholar
- Liu Y, Rouiller EM (1999) Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp Brain Res 128(1–2):149–159PubMedCrossRefGoogle Scholar
- Loubinoux I, Carel C, Pariente J, Dechaumont S, Albucher JF, Marque P et al (2003) Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage 20(4):2166–2180PubMedCrossRefGoogle Scholar
- Lu MT, Preston JB, Strick PL (1994) Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J Comp Neurol 341(3):375–392PubMedCrossRefGoogle Scholar
- Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311(4):463–482PubMedCrossRefGoogle Scholar
- 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(1):114–140PubMedCrossRefGoogle Scholar
- Maier MA, Olivier E, Baker SN, Kirkwood PA, Morris T, Lemon RN (1997) Direct and indirect corticospinal control of arm and hand motoneurons in the squirrel monkey (Saimiri sciureus). J Neurophysiol 78(2):721–733PubMedGoogle Scholar
- Maier MA, Illert M, Kirkwood PA, Nielsen J, Lemon RN (1998) Does a C3-C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey. J Physiol 511(Pt 1):191–212PubMedCrossRefGoogle Scholar
- Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18(2):125–136PubMedCrossRefGoogle Scholar
- 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(3):281–298PubMedCrossRefGoogle Scholar
- Matelli M, Luppino G, Fogassi L, Rizzolatti G (1989) Thalamic input to inferior area 6 and area 4 in the macaque monkey. J Comp Neurol 280(3):468–488PubMedCrossRefGoogle Scholar
- Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311(4):445–462PubMedCrossRefGoogle Scholar
- Matsuzaka Y, Tanji J (1996) Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. J Neurophysiol 76(4):2327–2342PubMedGoogle Scholar
- 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(3):653–662PubMedGoogle Scholar
- McKiernan BJ, Marcario JK, Karrer JH, Cheney PD (1998) Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80(4):1961–1980PubMedGoogle Scholar
- McNeal DW, Darling WG, Ge J, Stilwell-Morecraft KS, Solon KM, Hynes SM et al (2010) Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury. J Comp Neurol 518(5):586–621PubMedCrossRefGoogle Scholar
- Miyai I, Yagura H, Hatakenaka M, Oda I, Konishi I, Kubota K (2003) Longitudinal optical imaging study for locomotor recovery after stroke. Stroke 34(12):2866–2870PubMedCrossRefGoogle Scholar
- Morecraft RJ, Van Hoesen GW (1992) Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: evidence for somatotopy in areas 24c and 23c. J Comp Neurol 322(4):471–489PubMedCrossRefGoogle Scholar
- Munk H (1881) Uber die Funktionen der Grosshirnrinde. In: Hirshwald A (ed) Gesammelte Mitteilungen aus den Jahren. Hirshwald, Berlin, pp 1877–1880Google Scholar
- Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G (1997) Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol 78(4):2226–2230PubMedGoogle Scholar
- Nudo RJ, Masterton RB (1989) Descending pathways to the spinal cord: II. Quantitative study of the tectospinal tract in 23 mammals. J Comp Neurol 286(1):96–119PubMedCrossRefGoogle Scholar
- Nudo RJ, Milliken GW (1996a) Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol 75(5):2144–2149Google Scholar
- Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM (1996b) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16(2):785–807Google Scholar
- Nudo RJ, Wise BM, SiFuentes F, Milliken GW (1996c) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272(5269):1791–1794CrossRefGoogle Scholar
- Ogden R, Franz SI (1917) On cerebral motor control: the recovery of function from experimentally produced hemiplegia. Psychbiol 1:33–50CrossRefGoogle Scholar
- Park MC, Belhaj-Saif A, Gordon M, Cheney PD (2001) Consistent features in the forelimb representation of primary motor cortex in rhesus macaques. J Neurosci 21(8):2784–2792PubMedGoogle Scholar
- Penfield W, Boldrey E (1937). Somatic motor and sensory representation in the cerebreal cortex of man as studied by electrical stimulation. Brain 60:389–443Google Scholar
- Phillips CG, Porter R (1977) Corticospinal neurones. Their role in movement. Monogr Physiol Soc 34:v–xii, 1–450PubMedGoogle Scholar
- Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6(3):342–353PubMedCrossRefGoogle Scholar
- Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11(6):663–672PubMedCrossRefGoogle Scholar
- Pierrot-Deseilligny E (1996) Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons. Prog Neurobiol 48(4–5):489–517PubMedCrossRefGoogle Scholar
- Pineiro R, Pendlebury ST, Smith S, Flitney D, Blamire AM, Styles P et al (2000) Relating MRI changes to motor deficit after ischemic stroke by segmentation of functional motor pathways. Stroke 31(3):672–679PubMedCrossRefGoogle Scholar
- Plautz EJ, Milliken GW, Nudo RJ (2000) Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74(1):27–55PubMedCrossRefGoogle Scholar
- Porter R (1985) The corticomotoneuronal component of the pyramidal tract: corticomotoneuronal connections and functions in primates. Brain Res 357(1):1–26PubMedGoogle Scholar
- Prabhu G, Shimazu H, Cerri G, Brochier T, Spinks RL, Maier MA et al (2009) Modulation of primary motor cortex outputs from ventral premotor cortex during visually guided grasp in the macaque monkey. J Physiol 587(Pt 5):1057–1069PubMedCrossRefGoogle Scholar
- Preuss TM, Stepniewska I, Kaas JH (1996) Movement representation in the dorsal and ventral premotor areas of owl monkeys: a microstimulation study. J Comp Neurol 371(4):649–676PubMedCrossRefGoogle Scholar
- Ralston DD, Ralston HJ 3rd (1985) The terminations of corticospinal tract axons in the macaque monkey. J Comp Neurol 242(3):325–337PubMedCrossRefGoogle Scholar
- Rathelot JA, Strick PL (2006) Muscle representation in the macaque motor cortex: an anatomical perspective. Proc Natl Acad Sci U S A 103(21):8257–8262PubMedCrossRefGoogle Scholar
- Rathelot JA, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A 106(3):918–923PubMedCrossRefGoogle Scholar
- Recanzone GH, Merzenich MM, Jenkins WM (1992a) Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. J Neurophysiol 67(5):1057–1070Google Scholar
- Recanzone GH, Jenkins WM, Hradek GT, Merzenich MM (1992b) Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. J Neurophysiol 67(5):1015–1030Google Scholar
- Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992c) Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. J Neurophysiol 67(5):1031–1056Google Scholar
- Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106(Pt 3):655–673PubMedCrossRefGoogle Scholar
- Rizzolatti G, Camarda R, Fogassi L, 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(3):491–507PubMedCrossRefGoogle Scholar
- Rizzolatti G, Gentilucci M, Camarda RM, Gallese V, Luppino G, Matelli M et al (1990) Neurons related to reaching-grasping arm movements in the rostral part of area 6 (area 6a beta). Exp Brain Res 82(2):337–350PubMedCrossRefGoogle Scholar
- Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M (1994) Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res 102(2):227–243PubMedCrossRefGoogle Scholar
- Sakai ST, Stepniewska I, Qi HX, Kaas JH (2000) Pallidal and cerebellar afferents to pre-supplementary motor area thalamocortical neurons in the owl monkey: a multiple labeling study. J Comp Neurol 417(2):164–180PubMedCrossRefGoogle Scholar
- Schieber MH (2000) Inactivation of the ventral premotor cortex biases the laterality of motoric choices. Exp Brain Res 130(4):497–507PubMedCrossRefGoogle Scholar
- Schieber MH (2001) Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 86(5):2125–2143PubMedGoogle Scholar
- Schieber MH, Hibbard LS (1993) How somatotopic is the motor cortex hand area? Science 261(5120):489–492PubMedCrossRefGoogle Scholar
- Schieber MH, Poliakov AV (1998) Partial inactivation of the primary motor cortex hand area: effects on individuated finger movements. J Neurosci 18(21):9038–9054PubMedGoogle Scholar
- Schmidlin E, Brochier T, Maier MA, Kirkwood PA, Lemon RN (2008) Pronounced reduction of digit motor responses evoked from macaque ventral premotor cortex after reversible inactivation of the primary motor cortex hand area. J Neurosci 28(22):5772–5783PubMedCrossRefGoogle Scholar
- Scott SH, Sergio LE, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol 78(5):2413–2426PubMedGoogle Scholar
- Seitz RJ, Kleiser R, Butefisch CM (2005) Reorganization of cerebral circuits in human brain lesion. Acta Neurochir Suppl 93:65–70PubMedCrossRefGoogle Scholar
- Shima K, Mushiake H, Saito N, Tanji J (1996) Role for cells in the presupplementary motor area in updating motor plans. Proc Natl Acad Sci U S A 93(16):8694–8698PubMedCrossRefGoogle Scholar
- 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(5):1200–1211PubMedCrossRefGoogle Scholar
- Shinoda Y, Zarzecki P, Asanuma H (1979) Spinal branching of pyramidal tract neurons in the monkey. Exp Brain Res 34(1):59–72PubMedCrossRefGoogle Scholar
- Shinoda Y, Futami T, Kano M (1985) Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. II. Input-output organization of single thalamocortical neurons in the ventrolateral thalamus. Neurosci Res 2(3):157–180PubMedCrossRefGoogle Scholar
- Shinoda Y, Yamaguchi T, Futami T (1986) Multiple axon collaterals of single corticospinal axons in the cat spinal cord. J Neurophysiol 55(3):425–448PubMedGoogle Scholar
- Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330(2):238–271PubMedCrossRefGoogle Scholar
- Strick PL, Preston JB (1982) Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. J Neurophysiol 48(1):150–159PubMedGoogle Scholar
- Takada M, Tokuno H, Hamada I, Inase M, Ito Y, Imanishi M et al (2001) Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey. Eur J Neurosci 14(10):1633–1650PubMedCrossRefGoogle Scholar
- Tanji J, Okano K, Sato KC (1988) Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol 60(1):325–343PubMedGoogle Scholar
- Vogt C, Vogt O (1919) Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol (Leipz.) 25:279–461Google Scholar
- Von Bonin G, Bailey P (1947) The neocortex of Macaca Mulatta, vol 136. University of Illinois Press, UrbanaGoogle Scholar
- Wiesendanger R, Wiesendanger M (1985) The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (macaca fascicularis). Exp Brain Res 59(1):91–104PubMedGoogle Scholar
- Woolsey CN, Settlage PH, Meyer DR, Spencer W, Hamuy TP, Travis AM (1952) Patterns of localization in precentral and “supplementary” motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30:238–264PubMedGoogle Scholar
- Zhu LL, Lindenberg R, Alexander MP, Schlaug G (2010) Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke 41(5):910–915PubMedCrossRefGoogle Scholar