Advertisement

The Molecular Basis of Experience-Dependent Motor System Development

Conference paper
Part of the Advances in Experimental Medicine and Biology book series (volume 782)

Abstract

Neurons in the vertebrate nervous skystem acquire their mature features over an extended period in prenatal and early postnatal life. The interaction of the organism with its environment (“experience”) has been shown to profoundly influence sensory neuron development. Approximately, over the past two decades, it has become increasingly clear that motor system development is also experience dependent. Glutamate receptors of the N-methyl-D-aspartate (NMDA) subtype have been implicated in both sensory and motor system experience-dependent development. An additional molecular mechanism involves the GluA1 subunit of the 2-amino-3-(5-methyl-3-oxo-1,2-oxazol-4-yl)propanoic acid (AMPA) subtype glutamate receptors. GluA1-dependent development operates in an NMDA-R-independent manner and uses a distinct set of signaling molecules. The synapse-associated protein of 97 kDa molecular weight (SAP97) is the key. A deeper understanding of how experiences guide motor system development may lead to new ways to improve function after central nervous system insult.

Keywords

Green Fluorescent Protein Motor Neuron Dendrite Growth Dendritic Tree Segmental Spinal Cord 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported in the past by the US Public Health Service (NS29837). We thank R. Sprengel, P Seeburg, and R. Huganir for several of the murine strains used in these studies.

References

  1. Aizawa H, Hu SC, Bobb K, Balakrishnan K, Ince G, Gurevich I et al (2004) Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science 303(5655):197–202PubMedCrossRefGoogle Scholar
  2. Altman J, Sudarshan K (1975) Postnatal development of locomotion in the laboratory rat. Animal Behavior 23:896–920CrossRefGoogle Scholar
  3. Bannerman DM, Deacon RM, Brady S, Bruce A, Sprengel R, Seeburg PH et al (2004) A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav Neurosci 118(3):643–647PubMedCrossRefGoogle Scholar
  4. Barbeau H, Rossignol S (1987) Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412:84–95PubMedCrossRefGoogle Scholar
  5. Bi G, Poo M (2001) Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci 24:139–166PubMedCrossRefGoogle Scholar
  6. Cai C, Coleman SK, Niemi K, Keinanen K (2002) Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif. J Biol Chem 277(35):31484–31490PubMedCrossRefGoogle Scholar
  7. Carriedo SG, Yin HZ, Weiss JH (1996) Motor neurons are selectively vulnerable to AMPA/KA receptor-mediated injury in vitro. J Neurosci 16:4069–4079PubMedGoogle Scholar
  8. Chen SX, Tari PK, She K, Haas K (2010) Neurexin-neuroligin cell adhesion complexes contribute to synaptotropic dendritogenesis via growth stabilization mechanisms in vivo. Neuron 67(6):967–983PubMedCrossRefGoogle Scholar
  9. Chklovskii DB (2004) Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43(5):609–617PubMedGoogle Scholar
  10. Cline HT (2001) Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11(1):118–126PubMedCrossRefGoogle Scholar
  11. Cline H, Haas K (2008) The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol 586(6):1509–1517PubMedCrossRefGoogle Scholar
  12. Cline HT, Debski EA, Constantine-Paton M (1987) N-methyl-D-aspartate receptor antagonist desegregates eye-specific columns. PNAS 84:4342–4345PubMedCrossRefGoogle Scholar
  13. Constantine-Paton M, Cline HT, Debski E (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13:129–154PubMedCrossRefGoogle Scholar
  14. Cramer KS, Angelucci A, Hahm JO, Bogdanov MB, Sur M (1996) A role for nitric oxide in the development of the ferret retinogeniculate projection. J Neurosci 16:7995–8004PubMedGoogle Scholar
  15. Curfs MHJM, Gribnau AAM, Dideren PJWC (1993) Postnatal maturation of the dendritic fields of motoneuron pools supplying flexor and extensor muscles of the distal forelimb in the rat. Development 117:535–541PubMedGoogle Scholar
  16. Curfs MHJM, Gribnau AAM, Dederen PJWC (1994) Selective elimination of transient corticospinal projections in the rat cervical spinal cord gray matter. Dev Brain Res 78:182–190CrossRefGoogle Scholar
  17. Dierssen M, Ramakers GJ (2006) Dendritic pathology in mental retardation: from molecular genetics to neurobiology. Genes Brain Behav 5(Suppl 2):48–60PubMedGoogle Scholar
  18. Dietz V, Colombo G, Jensen L, Baumgartner L (1995) Locomotor capacity of spinal cord in paraplegic patients. Ann Neurol 37(5):574–582PubMedCrossRefGoogle Scholar
  19. Donatelle JM (1977) Growth of the Corticospinal tract and the development of placing reactions in the postnatal rat. J Comp Neurol 175:207–232PubMedCrossRefGoogle Scholar
  20. Edgerton VR, de Leon RD, Tillakaratne N, Recktenwald MR, Hodgson JA, Roy RR (1997) Use-dependent plasticity in spinal stepping and standing. Adv Neurol 72:233–247PubMedGoogle Scholar
  21. Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR (2004) Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci 27:145–167PubMedCrossRefGoogle Scholar
  22. Engert F, Tao HW, Zhang LI, Poo MM (2002) Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419(6906):470–475PubMedCrossRefGoogle Scholar
  23. Fung J, Stewart JE, Barbeau H (1990) The combined effects of clonidine and cyproheptadine with interactive training on the modulation of locomotion in spinal cord injured subjects. J Neurol Sci 100(1–2):85–93PubMedCrossRefGoogle Scholar
  24. Gao FB, Bogert BA (2003) Genetic control of dendritic morphogenesis in Drosophila. Trends Neurosci 26(5):262–268PubMedCrossRefGoogle Scholar
  25. Gaudilliere B, Konishi Y, de la Iglesia N, Yao G, Bonni A (2004) A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41(2):229–241PubMedCrossRefGoogle Scholar
  26. Gazula VR, Roberts M, Luzzio C, Jawad AF, Kalb RG (2004) Effects of limb exercise after spinal cord injury on motor neuron dendrite structure. J Comp Neurol 476(2):130–145PubMedCrossRefGoogle Scholar
  27. Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 10:77–98CrossRefGoogle Scholar
  28. Goold CP, Nicoll RA (2011) Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron 68(3):512–528CrossRefGoogle Scholar
  29. Ha S, Redmond L (2008) ERK mediates activity dependent neuronal complexity via sustained activity and CREB-mediated signaling. Dev Neurobiol 68(14):1565–1579PubMedCrossRefGoogle Scholar
  30. Hume RI, Purves D (1981) Geometry of neonatal neurons and the regulation of synapse elimination. Nature 293:469–471PubMedCrossRefGoogle Scholar
  31. Inglis FM, Furia F, Zuckerman KE, Strittmatter SM, Kalb RG (1998) The role of nitric oxide and NMDA receptors in the development of motor neuron dendrites. J Neurosci 18:10493–10501PubMedGoogle Scholar
  32. Inglis FM, Zuckerman KE, Kalb RG (2000) Experience-dependent development of spinal motor neurons. Neuron 26:299–305PubMedCrossRefGoogle Scholar
  33. Inglis FM, Crockett R, Korada S, Abraham WC, Hollmann M, Kalb RG (2002) The AMPA receptor GluR1 regulates dendritic architecture of motor neurons. J Neurosci 22:8042–8051PubMedGoogle Scholar
  34. Jakowec MW, Fox AJ, Martin LJ, Kalb RG (1995a) Quantitative and Qualitative Changes in AMPA Receptor Expression During Spinal Cord Development. Neuroscience 67:893–907CrossRefGoogle Scholar
  35. Jakowec MW, Yen L, Kalb RG (1995b) In situ hybridization analysis of AMPA receptor subunit gene expression in the developing rat spinal cord. Neuroscience 67:909–920CrossRefGoogle Scholar
  36. Jan YN, Jan LY (2003) The control of dendrite development. Neuron 40(2):229–242PubMedCrossRefGoogle Scholar
  37. Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M (2005) Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J Neurosci 25(49):11300–11312PubMedCrossRefGoogle Scholar
  38. Jeong GB, Werner M, Gazula VR, Itoh T, Roberts M, David S et al (2006) Bi-directional control of motor neuron dendrite remodeling by the calcium permeability of AMPA receptors. Mol Cell Neurosci 32(3):299–314PubMedCrossRefGoogle Scholar
  39. Kalb RG (1994) Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120:3063–3071PubMedGoogle Scholar
  40. Kalb RG (2003) Getting the spinal cord to think for itself. Arch Neurol 60(6):805–808PubMedCrossRefGoogle Scholar
  41. Katz LC, Constantine-Paton M (1988) Relationships between segregated afferents and postsynaptic neurons in the optic tectum of three-eyed frogs. J Neurosci 8:3160–3180PubMedGoogle Scholar
  42. Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10(10):981–991PubMedCrossRefGoogle Scholar
  43. Kim CH, Takamiya K, Petralia RS, Sattler R, Yu S, Zhou W et al (2005) Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat Neurosci 8(8):985–987PubMedCrossRefGoogle Scholar
  44. Kleinschmidt A, Bear MF, Singer W (1987) Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238:355–358PubMedCrossRefGoogle Scholar
  45. Kumar V, Zhang MX, Swank MW, Kunz J, Wu GY (2005) Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25(49):11288–11299PubMedCrossRefGoogle Scholar
  46. Li Z, Van Aelst L, Cline HT (2000) Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci 3(3):217–225PubMedCrossRefGoogle Scholar
  47. Li Z, Aizenman CD, Cline HT (2002) Regulation of rho GTPases by crosstalk and neuronal activity in vivo. Neuron 33(5):741–750PubMedCrossRefGoogle Scholar
  48. Li S, Zhang C, Takemori H, Zhou Y, Xiong ZQ (2009) TORC1 regulates activity-dependent CREB-target gene transcription and dendritic growth of developing cortical neurons. J Neurosci 29(8):2334–2343PubMedCrossRefGoogle Scholar
  49. Lin YC, Koleske AJ (2010) Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 33:349–378PubMedCrossRefGoogle Scholar
  50. Lindsay AD, Greer JJ, Feldman JL (1991) Phrenic Motoneuron Morphology in the Neonatal Rat. J Comp Neurol 308:169–179PubMedCrossRefGoogle Scholar
  51. Lovely RG, Gregor RJ, Roy RR, Edgerton VR (1990) Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res 514:206–218PubMedCrossRefGoogle Scholar
  52. Lu B (2003) Pro-region of neurotrophins: role in synaptic modulation. Neuron 39(5):735–738PubMedCrossRefGoogle Scholar
  53. McAllister AK, Katz LC, Lo DC (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17(6):1057–1064PubMedCrossRefGoogle Scholar
  54. McAllister AK, Katz LC, Lo DC (1997) Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendrite growth. Neuron 18:767–778PubMedCrossRefGoogle Scholar
  55. Morais Cabral JH, Petosa C, Sutcliffe MJ, Raza S, Byron O, Poy F et al (1996) Crystal structure of a PDZ domain. Nature 382(6592):649–652PubMedCrossRefGoogle Scholar
  56. Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS et al (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science 321(5886):218–223PubMedCrossRefGoogle Scholar
  57. Núñez-Abades PA, He F, Barrionuevo G, Cameron WE (1994) Morphology of developing rat genioglossal motoneurons studied in vitro: changes in length, branching pattern, and spatial distribution of dendrites. J Comp Neurol 339:401–420PubMedCrossRefGoogle Scholar
  58. Palmer CL, Cotton L, Henley JM (2005) The molecular pharmacology and cell biology of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol Rev 57(2):253–277PubMedCrossRefGoogle Scholar
  59. Pellis V, Pellis S, Teitelbaum P (1991) A descriptive analysis of the postnatal development of contact-righting in rats (Rattus norvegicus). Devel Psychobiol 24(4):237–263CrossRefGoogle Scholar
  60. Peng YR, He S, Marie H, Zeng SY, Ma J, Tan ZJ et al (2009) Coordinated changes in dendritic arborization and synaptic strength during neural circuit development. Neuron 61(1):71–84PubMedCrossRefGoogle Scholar
  61. Redmond L, Oh SR, Hicks C, Weinmaster G, Ghosh A (2000) Nuclear Notch1 signaling and the regulation of dendritic development. Nat Neurosci 3(1):30–40PubMedCrossRefGoogle Scholar
  62. Redmond L, Kashani AH, Ghosh A (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34(6):999–1010PubMedCrossRefGoogle Scholar
  63. Rossignol S (2000) Locomotion and its recovery after spinal injury. Curr Opin Neurobiol 10:708–716PubMedCrossRefGoogle Scholar
  64. Ruthazer ES, Akerman CJ, Cline HT (2003) Control of axon branch dynamics by correlated activity in vivo. Science 301(5629):66–70PubMedCrossRefGoogle Scholar
  65. Sato J, Shimazu D, Yamamoto N, Nishikawa T (2008) An association analysis of synapse-associated protein 97 (SAP97) gene in schizophrenia. J Neural Transm 115(9):1355–1365PubMedCrossRefGoogle Scholar
  66. Seebach BS, Ziskind-Conhaim L (1994) Formation of transient inappropriate sensorimotor synapses in developing rat spinal cord. J Neurosci 14:4520–4528PubMedGoogle Scholar
  67. Shalizi A, Gaudilliere B, Yuan Z, Stegmuller J, Shirogane T, Ge Q et al (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311(5763):1012–1017PubMedCrossRefGoogle Scholar
  68. Shatz CJ (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745–756PubMedCrossRefGoogle Scholar
  69. Sheng M, Sala C (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1–29PubMedCrossRefGoogle Scholar
  70. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613–643PubMedCrossRefGoogle Scholar
  71. Sin WC, Haas K, Ruthazer ES, Cline HT (2002) Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419(6906):475–480PubMedCrossRefGoogle Scholar
  72. Snider WD, Zhang L, Yusoof S, Gorukanti N, Tsering C (1992) Interactions between dorsal root axons and their target motor neurons in developing mammalian spinal cord. J Neurosci 12(9):3494–3508PubMedGoogle Scholar
  73. Stegenga SL, Kalb RG (2001) Developmental regulation of N-methyl-D-aspartate: and kainate-type glutamate receptor expression in the rat spinal cord. Neuroscience 105:499–507PubMedCrossRefGoogle Scholar
  74. Stuart G, Spruston N, Hausser M (1999) Dendrites. Oxford: Oxford University PressGoogle Scholar
  75. Thyagarajan A, Ting AY (2010) Imaging activity-dependent regulation of neurexin-neuroligin interactions using trans-synaptic enzymatic biotinylation. Cell 143(3):456–469PubMedCrossRefGoogle Scholar
  76. Toyooka K, Iritani S, Makifuchi T, Shirakawa O, Kitamura N, Maeda K et al (2002) Selective reduction of a PDZ protein, SAP-97, in the prefrontal cortex of patients with chronic schizophrenia. J Neurochem 83(4):797–806PubMedCrossRefGoogle Scholar
  77. Vandenberghe W, Robberecht W, Brorson JR (2000) AMPA receptor calcium permeability, GluR2 expression, and selective motoneuron vulnerability. J Neurosci 20(1):123–132PubMedGoogle Scholar
  78. Vaughn JE (1989) Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255–285PubMedCrossRefGoogle Scholar
  79. Vaughn JE, Barber RP, Sims TJ (1988) Dendritic development and preferential growth into synaptogenic fields: a quantitative study of Golgi-impregnated spinal motor neurons. Synapse 2(1):69–78PubMedCrossRefGoogle Scholar
  80. Walton KD, Lieberman D, Llinas A, Begin M, Llinas RR (1992) Identification of a critical period for motor development in neonatal rats. Neuroscience 51:763–767PubMedCrossRefGoogle Scholar
  81. Walton KD, Harding S, Anschel D, Harris YT, Llinas R (2005) The effects of microgravity on the development of surface righting in rats. J Physiol 565:593–608PubMedCrossRefGoogle Scholar
  82. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V et al (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50(6):897–909PubMedCrossRefGoogle Scholar
  83. Wernig A, Muller S, Nanassy A, Cagol E (1995) Laufband therapy based on “rules of spinal locomotion” is effective in spinal cord injured persons. Eur J Neurosci 7:823–829PubMedCrossRefGoogle Scholar
  84. Wernig A, Nanassy A, Muller S (1998) Maintainance of locomotor ability following Laufband (treadmill) therapy in para- and tetraplegia persons: follow-up studies. Spinal Cord 36:744–749PubMedCrossRefGoogle Scholar
  85. Willatt L, Cox J, Barber J, Cabanas ED, Collins A, Donnai D et al (2005) 3q29 microdeletion syndrome: clinical and molecular characterization of a new syndrome. Am J Hum Genet 77(1):154–160PubMedCrossRefGoogle Scholar
  86. Wirz M, Colombo G, Dietz V (2001) Long term effects of locomotor training in spinal humans. J Neurol Neurosurg Psychiatry 71(1):93–96PubMedCrossRefGoogle Scholar
  87. Wu GY, Cline HT (1998) Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–225PubMedCrossRefGoogle Scholar
  88. Wu HH, Williams CV, McLoon SC (1994) Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 265:1593–1596PubMedCrossRefGoogle Scholar
  89. Wu GY, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4(2):151–158PubMedCrossRefGoogle Scholar
  90. Yu X, Malenka RC (2003) Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6(11):1169–1177PubMedCrossRefGoogle Scholar
  91. Zamanillo D, Sprengel R, Hvalby O, Hensen V, Burnashev N, Rozov A et al (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not spatial learning. Science 284:1805–1811PubMedCrossRefGoogle Scholar
  92. Zhang LI, Tao HW, Poo M (2000) Visual input induces long-term potentiation of developing retinotectal synapses. Nat Neurosci 3(7):708–715PubMedCrossRefGoogle Scholar
  93. Zhang L, Schessl J, Werner M, Bonnemann C, Xiong G, Mojsilovic-Petrovic J et al (2008) Role of GluR1 in activity-dependent motor system development. J Neurosci 28(40):9953–9968PubMedCrossRefGoogle Scholar
  94. Zhou W, Zhang L, Guoxiang X, Mojsilovic-Petrovic J, Takamaya K, Sattler R et al (2008) GluR1 controls dendrite growth through its binding partner, SAP97. J Neurosci 28(41):10220–10233PubMedCrossRefGoogle Scholar
  95. Zou DJ, Cline HT (1999) Postsynaptic calcium/calmodulin-dependent protein kinase II required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J Neurosci 19:8909–8919PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Neurology, Children’s Hospital of Philadelphia, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Research Institute and Division of Neurology, Department of Pediatrics, Children’s Hospital of Philadelphia, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations