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Roles of Synaptic Plasticity in Functional Recovery After Brain Injury

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Neurobiological and Psychological Aspects of Brain Recovery

Part of the book series: Contemporary Clinical Neuroscience ((CCNE))

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Abstract

Patients with brain injury or stroke suffer from sensory-motor disorder caused by the loss of function of damaged brain tissues. The goal of neurorehabilitation is to facilitate the recovery of the impaired sensory-motor function through new learning in the remaining intact brain tissues. Synaptic plasticity, i.e., long-term potentiation and depression of synaptic transmission, and new synapse formation through axonal sprouting are assumed to underlie such new learning. To further elucidate roles of synaptic plasticity in neurorehabilitation, four items are addressed in this chapter. First, the characteristics of synaptic plasticity in the intact hippocampus, cerebellum, and red nucleus are reviewed. Second, the spinal, cerebellar, and cerebral mechanisms underlying the recovery of grasping or gripping movement after unilateral spinal cord injury are discussed as an experimental model of neurorehabilitation of motor function. Third, the neural mechanisms underlying the recovery of somatosensory and vestibular functions are discussed as an experimental model of the neurorehabilitation of sensory function after injury of their pathways in the central or peripheral nervous system. Finally, recent progress in neurorehabilitation techniques, noninvasive transcranial brain stimulation, neuroprosthesis, and regenerative medicine, including the induced pluripotent stem cell technology, is reviewed in relation to synaptic plasticity.

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References

  • Akaneya Y, Tsumoto T, Hatanaka H. Brain-derived neurotrophic factor blocks long-term depression in rat visual cortex. J Neurophysiol. 1996;76:4198–201.

    CAS  PubMed  Google Scholar 

  • Akaneya Y, Tsumoto T, Kinoshita S, Hatanaka H. Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J Neurosci. 1997;17:6707–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allum JH. Recovery of vestibular ocular reflex function and balance control after a unilateral peripheral vestibular deficit. Front Neurol. 2012;3:83. https://doi.org/10.3389/fneurol.00083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alstermark B, Ekerot CF. The lateral reticular nucleus: a precerebellar centre providing the cerebellum with overview and integration of motor functions at system level. A new hypothesis. J Physiol Lond. 2013;591:5453–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alstermark B, Isa T. Circuits for skilled reaching and grasping. Annu Rev Neurosci. 2012;35:559–78.

    CAS  PubMed  Google Scholar 

  • Alstermark B, Lundberg A. The C3-C4 propriospinal system: target-reaching and food-taking. In: Jami L, Pierrot-Deseilligny E, Zytnicki E, editors. Muscle afferents and spinal control of movement. Oxford: Pergamon Press; 1992. p. 327–54.

    Google Scholar 

  • Alstermark B, Pettersson L-G. Endogenous plasticity in neuro-rehabilitation following partial spinal cord lesions. Front Neurosci. 2014a;8:59. https://doi.org/10.3389/fnins.2014.00059.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alstermark B, Pettersson L-G. Skilled reaching and grasping in the rat: lacking of the effects corticospinal lesion. Front Neurol. 2014b;5:103. https://doi.org/10.3389/fneur.00103.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alstermark B, Lindström S, Lundberg A, Sybirska E. Ascending projection to the lateral reticular nucleus from C3-C4 propriospinal neurons also projecting to forelimb motoneurones. Exp Brain Res. 1981;42:282–98.

    CAS  PubMed  Google Scholar 

  • Alstermark B, Lundberg A, Pettersson L-G, Tantisira B, Walkowska M. Motor recovery after serial spinal cord lesions of defined descending pathways in cats. Neurosci Res. 1987;5:68–73.

    CAS  PubMed  Google Scholar 

  • Alstermark B, Isa T, Ohki Y, Saito Y. Disynaptic pyramidal excitation in forlimb motoneurons mediated via C(3)-C(4) propriospinal neurons in the Macaca fuscata. J Neurophysiol. 1999;82:3580–5.

    CAS  PubMed  Google Scholar 

  • Alstermark B, Pettersson LG, Nishimura Y, Yoshino-Saito K, Tsuboi F, Takahashi M, Isa T. Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons. J Neurophysiol. 2011;106:122–6.

    CAS  PubMed  Google Scholar 

  • Azim E, Jiang J, Alsternmark B, Jessell T. Skilled reaching relies on a V2a propriospinal internal copy circuit. Nature. 2014;508:357–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aziz W, Wang W, Kasaf S, Alsayed AAM, Fukazawa Y, Shigemoto R. Distinct kinetics of synaptic formation and memory decay in massed and spaced learning. Proc Natl Acad Sci U S A. 2014;111:E195–202.

    Google Scholar 

  • Baker SN. The primate reticulospinal tract, hand function and functional recovery. J Physiol Lond. 2011;589:5603–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new interspinal circuit in adult rats. Nat Neurosci. 2004;7:269–77.

    CAS  PubMed  Google Scholar 

  • Beraneck M, McKee JL, Aleisia M, Cullen KE. Asymmetric recovery in cerebellar deficient mice following unilateral labyrinthectomy. J Neurophysiol. 2008;100:945–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of perforant path. J Physiol Lond. 1973;232:331–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Courjon JH, Flandrin JM, Jennerod M, Schmid R. The role of the flocculus in vestibular compensation after hemilabyrinthectomy. Brain Res. 1982;239:251–7.

    CAS  PubMed  Google Scholar 

  • Dum RP, Strick PL. The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci. 1991;11:667–89.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dutheil S, Brezun JM, Leonard J, Lacour M, Tighilet B. Neurogenesis and astrogenesis contribution to recovery of vestibular function in the adult cat following unilateral vestibular neurectomy. Neuroscience. 2009;164:1444–56.

    CAS  PubMed  Google Scholar 

  • Eguchi K, Velicky P, Hollergeschwandtner E, Itakura M, Fukazawa Y, Danzi GJ, Shigemoto R. Advantages of acute slices prepared at physiological temperature in the characterization of synaptic functions. Front Cell Neurosci. 2020;14:63.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ekerot C-F. The lateral reticular nucleus in the cat. VII. Excitatory and inhibitory projections from the ipsilateral forelimb tract (iF tract). Exp Brain Res. 1990;79:120–8.

    CAS  PubMed  Google Scholar 

  • Faulstich M, van Alphen AM, Luo C, du Lac S, De Zeeuw CI. Oculomotor plasticity during vestibular compensation does not depend on cerebellar LTD. J Neurophysiol. 2006;96:1187–95.

    CAS  PubMed  Google Scholar 

  • Florence SL, Kaas JH. Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J Neurosci. 1995;15:8083–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G. Cortical mechanism for visual guidance of hand grasping movements in the monkey: a reversible inactivation study. Brain. 2001;124:571–86.

    CAS  PubMed  Google Scholar 

  • Frisch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B. Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implication for motor learning. Neuron. 2010;66:198–204.

    Google Scholar 

  • Fujito Y, Tsukahara N, Oda Y, Yoshida M. Formation of functional synapses in the adult cat red nucleus from the cerebrum following cross-innervation of forelimb flexor and extensor nerves. II. Analysis of newly appeared synaptic potentials. Exp Brain Res. 1982;45:13–8.

    CAS  PubMed  Google Scholar 

  • Funabiki K, Mishina M, Hirano T. Retarded vestibular compensation in mutant mice deficient in delta 2 glutamate receptor subunit. Neuroreport. 1995;7:189–92.

    CAS  PubMed  Google Scholar 

  • Gianotti C, Nunzi MG, Gispen WH, Corradetti R. Phosphorylation of the presynaptic protein B-50 (GAP-43) is increased during electrically induced long-term potentiation. Neuron. 1992;8:843–8.

    CAS  PubMed  Google Scholar 

  • Hashimoto Y, Honda T, Matsumura K, Nakao M, Soga K, Katano K, Yokota T, Mizusawa H, Nagao S, Ishikawa K. Quantitative evaluation of human cerebellum-dependent motor learning through prism adaptation of hand-reaching movement. PLoS One. 2015;10(3):e0119376.

    PubMed  PubMed Central  Google Scholar 

  • Higo N, Nishimura Y, Miura Y, Oishi T, Yoshino-Saito K, Takahashi M, Tsuboi F, Isa T. Increased expression of the growth-associated protein 43 gene in the sensorimotor cortex of macaque monkey after lesioning the lateral corticospinal tract. J Comp Neurol. 2009;516:493–506.

    CAS  PubMed  Google Scholar 

  • Honda T, Ito M. Development from Marr’s theory of the cerebellum to liquid state machine and beyond. In: Vaina LM, Passingham RE, editors. Computational theories and their implementations in the brain: the legacy of David Marr. Oxford, London: Oxford University Press; 2016.

    Google Scholar 

  • Honda T, Nagao S, Hashimoto Y, Ishikawa K, Yokota T, Mizusawa H, Ito M. Tandem internal models execute motor learning in the cerebellum. Proc Natl Acad Sci U S A. 2018;115:7426–33.

    Google Scholar 

  • Inoshita T, Hirano T. Occurrence of long-term depression in the cerebellar flocculus during adaptation of optokinetic response. Elife. 2018;7:e36209.

    PubMed  PubMed Central  Google Scholar 

  • Isa T. The brain is needed to cure spinal cord injury. Trends Neurosci. 2017;40:625–36.

    CAS  PubMed  Google Scholar 

  • Isa T. Dexterous hand movements and their recovery after central nervous system injury. Annu Rev Neurosci. 2019;42:315–35.

    CAS  PubMed  Google Scholar 

  • Isa T, Ohki Y, Seki K, Alstermark B. Properties of propriospinal neurons in the C3–C4 segments mediating disynaptic pyramidal excitation to forelimb motoneurons in the macaque monkey. J Neurophysiol. 2006;95:3674–85.

    PubMed  Google Scholar 

  • Ito M. Neurophysiological basis of the cerebellar motor control system. Int J Neurol. 1970;7:162–76.

    CAS  PubMed  Google Scholar 

  • Ito M. The cerebellum and neural control. New York: Raven; 1984.

    Google Scholar 

  • Ito M. Long-term depression. Annu Rev Neurosci. 1989;12:85–102.

    CAS  PubMed  Google Scholar 

  • Ito M. Cerebellar long-term depression—characterization, signal transduction and functional roles. Physiol Rev. 2001;81:1143–95.

    CAS  PubMed  Google Scholar 

  • Ito M. Cerebellar circuitry as a neuronal machine. Prog Neurobiol. 2006;78:272–303.

    PubMed  Google Scholar 

  • Ito M. The cerebellum: brain for an implicit self. New York: FT Press; 2012.

    Google Scholar 

  • Ito M, Kano M. Long-lasting depression of parallel fiber-Purkinje cell transmission by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett. 1982;33:253–8.

    CAS  PubMed  Google Scholar 

  • Ito M, Sakurai M, Tongroach P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cell. J Physiol Lond. 1982;324:113–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ito M, Yamaguchi K, Nagao S, Yamazaki T. Long-term depression as a model of cerebellar plasticity. Prog Brain Res. 2014;210:1–30.

    PubMed  Google Scholar 

  • Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, Kobayashi S, Yamasaki M, Momoshima S, Ishii H, Ando K, Tanioka Y, Tamaoki N, Nomura T, Toyama Y, Okano H. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res. 2005;80:182–90.

    CAS  PubMed  Google Scholar 

  • Jacobi A, Loy K, Schmalz AM, Hellsten M, Umemori H, Kerschensteiner M, Bareyre FM. FGF22 signaling regulates synapse formation during post-injury remodeling of the spinal cord. EMBO J. 2015;34:1231–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins WM, Mezenich MM, Ochs MT, Allard T, Guic-Robles E. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J Neurophysiol. 1990;63:82–104.

    CAS  PubMed  Google Scholar 

  • Jones EG. Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu Rev Neurosci. 2000;23:1–37.

    CAS  PubMed  Google Scholar 

  • Jorntell H, Ekerot C-F. Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron. 2002;34:797–806.

    CAS  PubMed  Google Scholar 

  • Jorntell H, Ekerot C-F. Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J Neurosci. 2003;23:9620–31.

    PubMed  PubMed Central  Google Scholar 

  • Kaas JH. Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci. 1991;14:137–67.

    CAS  PubMed  Google Scholar 

  • Kakegawa W, Katoh A, Narumi S, Miura E, Motohashi J, Takahashi A, Kohda K, Fukazawa Y, Yuzaki M, Matsuda S. Optogentic control of synaptic AMPA receptor endocytosis reveals roles of LTD in motor learning. Neuron. 2018;99:985–98.

    CAS  PubMed  Google Scholar 

  • Kamiyama T, Kameda H, Murabe N, Fukuda S, Yoshioka N, Mizukami H, Ozawa K, Sakurai M. Corticospinal tract development and spinal cord innervation differ between cervical and lumbar targets. J Neurosci. 2015;35:1181–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kano M, Iino K, Maekawa K, Kano MS. Optokinetic response of cells in the nucleus reticularis tegmenti pontis of the pigmented rabbits. Exp Brain Res. 1991;87:239–44.

    CAS  PubMed  Google Scholar 

  • Kano M, Rexhausen U, Dreessen J, Konnerth A. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory signals in cerebellar Purkinje cells. Nature. 1992;356:601–4.

    CAS  PubMed  Google Scholar 

  • Kawato M, Furukawa K, Suzuki R. A hierarchical neural-network model for control and learning of voluntary movement. Biol Cybern. 1987;57:169–85.

    CAS  PubMed  Google Scholar 

  • Kawato M, Ohmae S, Hoang H, Sanger T. 50 years since Marr, Albus, Ito models of the cerebellum. Neuroscience. 2021;461:151–74.

    Google Scholar 

  • Kelly RM, Strick PL. Cerebellar loops with motor cortex prefrontal cortex of a non-human primate. J Neurosci. 2003;23:8432–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamura K, Iwanami A, Nakamura M, Yamane J, Watanabe K, Suzuki Y, Miyazawa D, Shibata S, Funakoshi H, Miyatake S, Coffin RS, Nakamura T, Toyama Y, Okano H. Hepatocytic growth factor promotes endogenous repair and functional recovery after spinal cord injury. J Neurosci Res. 2007;85:2332–42.

    CAS  PubMed  Google Scholar 

  • Kitamura K, Fujiyoshi K, Yamane J, Toyota F, Hikishima K, Nomura T, Funakoshi H, Nakamura T, Aoki M, Toyama Y, Okano H, Nakamura M. Human hepatocyte growth factor promotes functional recovery in primates after spinal cord injury. PLoS One. 2011;6(11):e27706. https://doi.org/10.1371/journal.pone.0027706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamura K, Nagoshi N, Tsuji O, Matsumoto M, Okano H, Nakamura M. Application of hepatocytic growth factor for acute spnal iinjury. Int J Mol Sci. 2019;28:20

    Google Scholar 

  • Kobayashi Y, Okada Y, Itakura G, Iwai H, Nishimura S, Yasuda A, Nori S, Hikishima K, Konomi T, Fujiyoshi K, Tsuji O, Toyama Y, Yamanaka S, Nakamura M, Okano H. Pre-evaluated safe human iPSC-derived neural stem cells promote functional recovery after spinal cord injury in common marmoset without tumorgenicity. PLoS One. 2012;7(12):e52787. https://doi.org/10.1371/journal.pone.0052787.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacour M, Bernad-Demanze L. Interaction between vestibular compensation mechanisms and vestibular rehabilitation therapy: 10 recommendations for optimal functional therapy. Front Neurol. 2015;5:285. https://doi.org/10.3899/fneur.2014.00285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lang C, Bradley PM, Jacobi A, Kerschensteiner M, Bareyre FM. STAT3 promotes corticospinal remodeling and functional recovery after spinal cord injury. EMBO Rep. 2013;14:931–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrence DG, Kypers HGJM. The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain. 1968a;91:1–14.

    CAS  PubMed  Google Scholar 

  • Lawrence DG, Kypers HGJM. The functional organization of the motor system in the monkey. II. The effects of lesions of descending brain-stem pathway. Brain. 1968b;91:15–36.

    CAS  PubMed  Google Scholar 

  • Lev-Ram V, Wong ST, Storm DR, Tsien RY. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci U S A. 2002;99:8389–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li YX, Hashimoto T, Tokuyama W, Miyashita Y, Okuno H. Spatiotemporal dynamics of brain-derived neurotrophic factor mRNA induction in the vestibule-olivary network during vestibular compensation. J Neurosci. 2001a;21:2738–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li YX, Tokuyama W, Okuno H, Miyashita Y, Hashimoto T. Differential induction of brain-derived neurotrophic factor mRNA in rat inferior olive subregions following unilateral labyrinthectomy. Neuroscience. 2001b;106:385–94.

    CAS  PubMed  Google Scholar 

  • Liew SL, Santamecchi E, Buch ER, Cohen LG. Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery. Front Hum Neurosci. 2014;8:378. https://doi.org/10.3389/fnhum:00378.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maekawa K, Simpson JI. Climbing fiber responses evoked in the vestibulocerebellum of rabbit from visual system. J Neurophysiol. 1973;36:649–66.

    CAS  PubMed  Google Scholar 

  • Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol. 1984;224:591–605.

    CAS  PubMed  Google Scholar 

  • Mewes K, Cheney PD. Facilitation and suppression of wrist and digit muscles from single rubromotoneuronal cells in awake monkey. J Neurophysiol. 1991;66:1965–77.

    CAS  PubMed  Google Scholar 

  • Miyashita Y, Nagao S. Analysis of signal content of Purkinje cell responses to optokinetic stimulation in the rabbit cerebellar flocculus by selective lesions of brainstem pathway. Neurosci Res. 1984;1:223–41.

    CAS  PubMed  Google Scholar 

  • Miyashita Y, Ito M, Jastreboff PJ, Maekawa K, Nagao S. Effects upon eye movements of rabbits induced by severance of mossy fiber visual pathway to the cerebellar flocculus. Brain Res. 1980;198:210–5.

    CAS  PubMed  Google Scholar 

  • Mogilner A, Grossman JA, Ribary U, Joliot M, Volkmann J, Rapaport D, Beasley RW, Llinás RR. Somatosensory cortical plasticity in adult humans revealed by magnetoencephalography. Proc Natl Acad Sci U S A. 1993;90:3593–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murai N, Tsuji J, Ito J, Mishina M, Hirano T. Vestibular compensation in glutamate receptor delta-2 subunit knockout mice: dynamic property of vestibulo-ocular reflex. Eur Arch Otorhinolaryngol. 2004;261:82–6.

    PubMed  Google Scholar 

  • Murakami F, Fujito Y, Tsukahara N. Physiological properties of the newly formed cortico-rubral synapses of red nucleus neurons due to collateral sprouting. Brain Res. 1976;103:147–51.

    CAS  PubMed  Google Scholar 

  • Nagao S. Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic eye movements in pigmented rabbits. Exp Brain Res. 1983;53:36–46.

    CAS  PubMed  Google Scholar 

  • Nagao S. Ocular reflex adaptation as an experimental model of cerebellar learning – In memory of Masao Ito –. Neuroscience. 2021a;462:191–204.

    Google Scholar 

  • Nagao S. Role of the cerebellum in the acquisition and storage of memory of motor learning. In: Mizusawa H, Kakei S, editors. Cerebellum as a CNS hub (Contemporary clinical neuroscience). Berlin Heidelberg, New York: Springer-Nature; 2021b. p. 305–25.

    Google Scholar 

  • Namgung U, Matsuyama S, Routtenberg A. Long-term potentiation activates the GAP-43 promoter: selective participation of hippocampal mossy cells. Proc Natl Acad Sci U S A. 1997;94:11675–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nathan PW, Smith MC. Long descending tracts in man. 1. Review of present knowledge. Brain. 1955;78:248–303.

    CAS  PubMed  Google Scholar 

  • Nishimura Y, Isa T. Cortical and subcortical compensatory mechanisms after spinal cord injury in monkeys. Exp Neurol. 2012;235:152–61.

    PubMed  Google Scholar 

  • Nishimura Y, Onoe H, Morichika Y, Perfiliev S, Tsukada H, Isa T. Time-dependent central compensatory mechanisms of finger dexterity after spinal cord injury. Science. 2007;318:1150–5.

    CAS  PubMed  Google Scholar 

  • Nishimura Y, Morichika Y, Isa T. A subcortical oscillatory network after spinal cord injury. Brain. 2009;132:709–21.

    PubMed  PubMed Central  Google Scholar 

  • Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, Nakamura M, Bregman BS, Koike M, Uchiyama Y, Toyama Y, Okano H. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res. 2002;69:925–33.

    CAS  PubMed  Google Scholar 

  • Okamoto T, Endo S, Shirao T, Nagao S. Role of cerebellar cortical protein synthesis in transfer of memory trace of cerebellum-dependent motor learning. J Neurosci. 2011a;31:8958–66.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto T, Shirao T, Shutoh F, Suzuki T, Nagao S. Post-training cerebellar cortical activity plays an important role for consolidation of memory of cerebellum-dependent motor learning. Neurosci Lett. 2011b;504:53–6.

    CAS  PubMed  Google Scholar 

  • Okano H, Yamanaka S. iPS cell technologies: significance and application to CNS regeneration and disease. Mol Brain. 2014;7:22. https://doi.org/10.1186/1756-6606-7-22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onodera S, Hicks TP. Carbocyanine dye usage in demarcating boundaries of the aged human red nucleus. PLoS One. 2010;5:e14430. https://doi.org/10.1371/journal.pone.0006623.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettersson L-G, Blagovechtchenski E, Perfiliev S, Krasnochokova E, Lundberg A. Recovery of food-taking in cats after lesions of the corticospinal (complete) and rubrospinal (complete and incomplete) tracts. Neurosci Res. 2000;38:109–12.

    CAS  PubMed  Google Scholar 

  • Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. Massive cortical regeneration after sensory deafferentiation in adult macaques. Science. 1991;252:1857–60.

    CAS  PubMed  Google Scholar 

  • Precht W. Neural operation in the vestibular system. In: Barlow HH, Konstanz EF, Grusser O-J, van der Loos H, editors. Study of brain function, vol. 2. Berlin Heidelberg, New York: Springer; 1977.

    Google Scholar 

  • Pugh JR, Raman IM. Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron. 2006;51:113–23.

    CAS  PubMed  Google Scholar 

  • Qi HX, Gharbawie OA, Wynne KW, Kaas JH. Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys. Behav Brain Res. 2013;252:363–76.

    PubMed  PubMed Central  Google Scholar 

  • Qi HX, Kaas JH, Reed JL. The reactivation of somatosensory cortex and behavioral recovery after sensory loss in mature primates. Front Syst Neurosci. 2014;8:84. https://doi.org/10.3389/fnsys.2014.00084.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raisman G. Formation of synapses in the adult after injury: similarities and differences between a peripheral and a central nervous site. Philos Trans R Soc Lond Ser B Biol Sci. 1977;278:349–59.

    CAS  Google Scholar 

  • Raisman G. What hope for repair of the brain? Ann Neurol. 1978;3:101–6.

    CAS  PubMed  Google Scholar 

  • Raisman G, Field PM. A quantitative investigation of the development of collateral innervation after partial deafferentation of septal nuclei. Brain Res. 1973;50:241–64.

    CAS  PubMed  Google Scholar 

  • Ramachandran VS. Behavioral and magnetoencephalographic correlations of plasticity in the adult human brain. Proc Natl Acad Sci U S A. 1993;90:10413–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rancillac A, Crepel F. Synapses between parallel fibers and stellate cells express long-term changes in synaptic efficacy in rat cerebellum. J Physiol Lond. 2004;554:707–20.

    CAS  PubMed  Google Scholar 

  • Recanzone GH, Allard TT, Jenkins WM, Merzenich MM. Receptive-field changes induced by peripheral nerve stimulation in SI of adult cats. J Neurophysiol. 1990;63:1213–25.

    CAS  PubMed  Google Scholar 

  • Rothwell JC. Plasticity in human motor system. Folia Phoniatr Logop. 2010;62:153–7.

    PubMed  Google Scholar 

  • Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, Nout YS, Roy RR, Miller DM, Beattie MS, Havton LA, Bresnahan JC, Edgerton VR, Tuszynski MH. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci. 2010;13:1505–1510.

    Google Scholar 

  • Sakurai M. Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J Physiol Lond. 1987;394:463–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanes JR, Jessel TM. Chapter 57: Repairing the damaged brain. In: Kandel ER, Schwartz JH, Jessel TM, Siegelbaum S, Hudspeth AJ, editors. Principles of neural science. 5th ed. New York: McGraw-Hill; 2012. p. 1284–305.

    Google Scholar 

  • Sano T, Kohyama-Koganeya Y, Kinoshita MO, Tatsukawa T, Shimizu C, Oshima E, Yamada K, Le TD, Akagi T, Tohyama K, Nagao S, Hirabayashi Y. Loss of GPRC5B impairs synapse formation of Purkinje cells with cerebellar nuclear neurons and disrupts cerebellar synaptic plasticity and motor learning. Neurosci Res. 2018;136:33–47.

    CAS  PubMed  Google Scholar 

  • Sasaki S, Isa T, Pettersson LG, Alstermark B, Naito K, Yoshimura K, Seki K, Ohki Y. Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. J Neurophysiol. 2004;92:3142–7.

    PubMed  Google Scholar 

  • Sawada M, Kato K, Kunieda T, Mikuni N, Miyamoto S, Onoe H, Isa T, Nishimura Y. Function of the nucleus accumbens in motor control during recovery after spinal cord injury. Science. 2015;350:98–101.

    CAS  PubMed  Google Scholar 

  • Scharfman HE, Goodman JH, Sollas AL. Action of brain-derived neurotrophic factor in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. J Neurosci. 1999;19:5619–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schonewille M, Gao Z, Boele H-J, Veloz MFV, Amerika WE, Simek AAM, De Jeu MT, Steinberg JP, Takamya K, Hoebeck FE, Liden DJ, Huiganir RL, De Zeeuw CI. Reevalatiing the role of LTD in motor learnibg. Neuron. 2011;70:43–50.

    Google Scholar 

  • Sczesny-Kaiser M, Hoffken O, Aach M, Cruciger O, Grasmucke D, Meindl R, Schildhauer TA, Schwenkreis P, Tegenthoff M. HAL exoskeleton training improves walking parameters and normalizes cortical excitability in primary somatosensory cortex in spinal cord injury patients. J Neuroeng Rehabil. 2015;12:68. https://doi.org/10.1186/s12984-015-0058-9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S. Memory trace of motor learning shifts from cerebellar cortex to nuclei for consolidation. Neuroscience. 2006;139:767–77.

    CAS  PubMed  Google Scholar 

  • Stanton PK, Sejnowski TJ. Associative long-term depression in the hippocampus induced by hebbian covariance. Nature. 1989;339:215–8.

    CAS  PubMed  Google Scholar 

  • Strick PL. Anatomical organization of multiple motor areas in the frontal lobe: implications for recovery of function. Adv Neurol. 1988;47:293–312.

    CAS  PubMed  Google Scholar 

  • Suzuki K, Elegheert J, Song I, Sasakura H, Senkov O, Matsuda K, Kekegawa W, Clayton AJ, Chang VT, Ferrer-Ferrer M, Miura E, Kausik R, Ikeno M, Morioka Y, Takeuchi Y, Shimada T, Otsuka S, Stoyanov S, Watanabe M, Takeuchi K, Dityatev A, Aricescu AR, Yuzaki M. A synthetic synaptic organizer proteins restores glutamatergic neuronal circuits. Science. 2020;369(6507):eabb4853.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka S, Kawaguchi SY, Shioi G, Hirano T. Long-term potentiation of inhibitory synaptic transmission onto cerebellar Purkinje neurons contributes to adaptation of vestibule-ocular reflex. J Neurosci. 2013;33:17209–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tighilet B, Brezun JM, Sylvie GD, Gaubert C, Lacour M. New neurons in the vestibular nuclei complex after unilateral vestibular neurectomy in the adult cat. Eur J Neurosci. 2007;25:47–58.

    PubMed  Google Scholar 

  • Tsuji O, Miura K, Okada Y, Fujiyoshi K, Mukaino M, Nagoshi N, Kitamura K, Kumagai G, Nishino M, Tomisato S, Higashi H, Nagai T, Katoh H, Kohda K, Matsuzaki Y, Yuzaki M, Ikeda E, Toyama Y, Nakamura M, Yamanaka S, Okano H. Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proc Natl Acad Sci U S A. 2010;107:12704–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukahara N, Fujito Y. Physiological evidence of new synapses from cerebrum in the red nucleus neurons following cross-union of forelimb nerve. Brain Res. 1976;106:184–8.

    CAS  PubMed  Google Scholar 

  • Tsukahara N, Hultborn H, Murakami F, Fujito Y. Electrophysiological study of formation of new synapses and collateral sprouting in red nucleus neurons after partial denervation. J Neurophysiol. 1975;38:1359–72.

    CAS  PubMed  Google Scholar 

  • Tsukahara N, Fujito Y, Oda Y, Maeda J. Formation of functional synapses in the adult cat red nucleus from the cerebrum following cross-innervating of forelimb flexor and extensor nerves. I. Appearance of new synaptic potentials. Exp Brain Res. 1982;45:1–12.

    CAS  PubMed  Google Scholar 

  • Wang W, Nakadate K, Masugi-Tokita M, Shutoh F, Aziz W, Tarusawa E, Lorincz A, Molner E, Kesaf S, Li Y-Q, Fukazawa Y, Nagao S, Shigemoto R. Distinct cerebellar engrams in short-term and long-term motor learning. Proc Natl Acad Sci U S A. 2014;111:E188–93.

    CAS  PubMed  Google Scholar 

  • Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain. 2003a;126:1430–48.

    CAS  PubMed  Google Scholar 

  • Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain. 2003b;126:2476–96.

    CAS  PubMed  Google Scholar 

  • Wessel MJ, Zimerman M, Hummel FC. Non-invasive brain stimulation: an interventional tool for enhancing behavioral training after stroke. Front Hum Neurosci. 2015;9:265. https://doi.org/10.3389/fuhum.2015.00265.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi K, Itohara S, Ito M. Reassessment of long-term depression in cerebellar Purkinje cells in mice carrying mutated GluA2 C terminus. Proc Natl Acad Sci U S A. 2016;113:10192–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki T, Nagao S. A computational mechanism for unified gain and timing control in the cerebellum. PLoS One. 2012;7:e33319. https://doi.org/10.1371/journal.pone.0033319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki T, Nagao S, Lennon W, Tanaka S. Modeling memory consolidation during posttraining periods in cerebellovestibular learning. Proc Natl Acad Sci U S A. 2015;112:3541–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimoto T, Shimizu I, Hiroi Y, Kawaki M, Nagasawa M. Feasibility and efficacy of high-speed gait training with a voluntary driven exoskeleton robot for gait and balance dysfunction in patients with chronic stroke: nonrandomized pilot study with concurrent control. Int J Rehabil Res. 2015;36:338–43.

    Google Scholar 

  • Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN. Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkeys. Brain. 2012;135:2277–89.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors are grateful to Dr. Takeru Honda (Motor Disorders Project, Tokyo Metropolitan Institute of Medical Science) for his helpful comments on this manuscript. Dr. Masao Ito passed away on 18th in December, 2018.

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Authors and Affiliations

  1. Nozomi Higher Brain Function Laboratory, Nozomi Hospital, Komuro, Ina, Saitama, Japan

    Soichi Nagao

  2. RIKEN Brain Science Institute, Wako, Saitama, Japan

    Masao Ito

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  1. Soichi Nagao
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  2. Masao Ito
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Correspondence to Soichi Nagao .

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  1. Santa Lucia Foundation IRCCS, Rome, Italy

    Laura Petrosini

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Nagao, S., Ito, M. (2023). Roles of Synaptic Plasticity in Functional Recovery After Brain Injury. In: Petrosini, L. (eds) Neurobiological and Psychological Aspects of Brain Recovery. Contemporary Clinical Neuroscience. Springer, Cham. https://doi.org/10.1007/978-3-031-24930-3_8

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