Conversion of functional synapses into silent synapses in the trigeminal brainstem after neonatal peripheral nerve transection

Journal of Neuroscience

Volumn 27, Issue 18, 2007, Pages 4929-4934

  Lo, Fu Sun ^a   Erzurumlu, Reha S ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptors; Barrelettes; Infraorbital nerve; NMDA receptors; Principal sensory nucleus; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; GLYCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; ELECTROSTIMULATION; EXOCYTOSIS; IN VITRO STUDY; NERVE TRANSECTION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PERIPHERAL NERVE; PRIORITY JOURNAL; RAT; SENSORY STIMULATION; SYNAPTIC TRANSMISSION; TRIGEMINAL NERVE; VOLTAGE CLAMP;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; DENERVATION; PERIPHERAL NERVES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SYNAPSES; TRIGEMINAL NERVE;

EID: 34247899166     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5342-06.2007     Document Type: Article

References (51)

1. Arends JJ, Jacquin MF (1993) Lucifer Yellow staining in fixed brain slices: optimal methods and compatibility with somatotopic markers in neonatal brain. J Neurosci Methods 50:321-339.
2. Arvidsson J (1979) An ultrastructural study of transganglionic degeneration in the main sensory trigeminal nucleus of the rat. J Neurocytol 8:31-45.
3. Ashby MC, De La Rue SA, Ralph GS, Uney J, Collingridge GL, Henley JM (2004) Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24:5172-5176.
4. Baldi A, Calia E, Ciampini A, Riccio M, Vetuschi A, Persico AM, Keller F (2000) Deafferentation-induced apoptosis of neurons in thalamic somatosensory nuclei of the newborn rat: critical period and rescue from cell death by peripherally applied neurotrophins. Eur J Neurosci 12:2281-2290.
5. Bates CA, Erzurumlu RS, Killackey HP (1982) Central correlates of peripheral pattern alterations in the trigeminal system of the rat. III. Neurons of the principal sensory nucleus. Brain Res 281:108-113.
6. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
7. Belford GR, Killackey HP (1979) The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 188:63-74.
8. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
9. Cabanes C, López de Armentia M, Viana F, Belmonte C (2002) Postnatal changes in membrane properties of mice trigeminal ganglion neurons. J Neurophysiol 87:2398-2407.
10. de Rivero Vaccari JC, Casey GP, Aleem S, Park WM, Corriveau RA. (2006) NMDA receptors promote survival in somatosensory relay nuclei by inhibiting Bax-dependent developmental cell death. Proc Natl Acad Sci USA 103:16971-16976.
11. Donoghue JP. (2002) Connecting cortex to machines: recent advances in brain interfaces. Nat Neurosci 5 Suppl:1085-1088.
12. Groc L, Gustafsson B, Hanse E (2006) AMPA signaling in nascent glutamatergic synapses: there and not there! Trends Neurosci 29:132-139.
13. Guido W, Lo F-S, Erzurumlu RS (2001) Synaptic plasticity in the trigeminal principal nucleus during the period of barrelette formation and consolidation. Dev Brain Res 132:97-102.
14. Henderson TA, Woolsey TA, Jacquin MF (1992) Infraorbital nerve blockade from birth does not disrupt central trigeminal pattern formation in the rat. Dev Brain Res 66:146-152.
15. Henderson TA, Rhoades RW, Bennett-Clarke CA, Osborne PA, Johnson EM, Jacquin MF (1993) NGF augmentation rescues trigeminal ganglion and principalis neurons, but not brainstem or cortical whisker patterns, after infraorbital nerve injury at birth. J Comp Neurol 336:243-260.
16. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
17. Iwasato T, Erzurumlu RS, Huerto PT, Sasaoka T, Ulupinar E, Tonegawa S (1997) NMDA receptor-dependent refinement of somatotopic maps. Neuron 19:1-20.
18. Kashiwagi K, Pahk AJ, Masuko T, Igarashi K, Williams K (1997) Block and modulation of N-methyl-D-aspartate receptors by polyamines and protons: role of amino acid residues in the transmembrane and pore forming regions of NR1 and NR2 subunits. Mol Pharmacol 52:701-713.
19. Killackey HP, Belford GR (1979) The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J Comp Neurol 183:285-303.
20. Killackey HP, Belford G, Ryugo R, Ryugo DK (1976) Anomalous organization of thalamocortical projections consequent to vibrissae removal in the newborn rat and mouse. Brain Res 104:309-315.
21. Kim HC, Chung MY (1999) Voltage-dependent sodium and calcium currents in acutely isolated adult rat trigeminal root ganglion neurons. J Neurophysiol 81:1123-1134.
22. Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, Natsume R, Watanabe M, Inoue Y, Yagi T, Aizawa S, Arakawa M, Takahashi T, Nakamura Y, Mori H, Mishina M (1996) Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor e2 subunit mutant mice. Neuron 16:333-344.
23. Lebedev MA, Nicolelis MA (2006) Brain-machine interfaces: past, present and future. Trends Neurosci 29:536-546.
24. Lee LJ, Lo F-S, Erzurumlu RS (2005) NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci 25:2304-2311.
25. Li Y, Erzurumlu RS, Chen C, Jhaveri S, Tonegawa S (1994) Whisker-related neuronal patterns fail to develop in the brainstem trigeminal nuclei of NMDAR1 knockout mice. Cell 76:427-437.
26. Liao D, Hessler NA, Malinow R (1995) Activity of postsynaptic silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
27. Lo F-S, Erzurumlu RS (2001) Neonatal deafferentation does not alter membrane properties of developing trigeminal principal sensory nucleus neurons. J Neurophysiol 85:1088-1096.
28. Lo F-S, Erzurumlu RS (2002) L-Type calcium channel-mediated plateau potentials in barrelette cells of the principal trigeminal nucleus during structural plasticity. J Neurophysiol 88:794-801.
29. Lo F-S, Mize RR (2001) Properties of LTD and LTP of retinocollicular synaptic transmission in the developing rat superior colliculus. Eur J Neurosci 15:1421-1432.
30. Lo F-S, Guido W, Erzurumlu RS (1999) Electrophysiological properties and synaptic responses of cells in the whisker representation area of the postnatal rat trigeminal principal sensory nucleus. J Neurophysiol 82:2765-2775.
31. Lu W, Constantine-Paton M (2004) Eye opening rapidly induces synaptic potentiation and refinement. Neuron 43:237-249.
32. Lu W-Y, Man H-Y, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29:243-254.
33. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5 21.
34. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
35. Miller MW, Kuhn P (1997) Neonatal transection of the infraorbital nerve increases the expression of protein related to neuronal death in the principal sensory nucleus of the trigeminal nerve. Brain Res 796:233-244.
36. Miller MW, al-Ghoul WM, Murtaugh M (1991) Expression of ALZ-50 immunoreactivity in the developing principal sensory nucleus of the trigeminal nerve: effect of transecting the infraorbital nerve. Brain Res 560:132-138.
37. Minnery BS, Simon DJ (2003) Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis. J Neurophysiol 89:40-56.
38. Rudhard Y, Kneussel M, Nassar MA, Rast GF, Annala AJ, Chen PE, Tigaret CM, Dean I, Roes J, Gibb AJ, Hunt SP, Schoepfer R (2003) Absence of Whisker-related pattern formation in mice with NMDA receptors lacking coincidence detection properties and calcium signaling. J Neurosci 23:2323-2332.
39. Sakurada K, Masu M, Nakanishi S (1993) Alteration of Ca2+ permeability and sensitivity to Mg2+ and channel blocker by a single amino acid substitution in the N-methyl-D-aspartate receptor. J Biol Chem 268:410-415.
40. Scheetz AJ, Constantine-Paton M (1994) Modulation of NMDA receptor function: implications for vertebrate neural development. FASEB J 8:745-752.
41. Schneggenburger R, Ascher P (1997) Coupling of permeation and gating in an NMDA-channel pore mutant. Neuron 18:167-177.
42. Sheng M, Lee SH (2003) AMPA receptor trafficking and synaptic plasticity: major unanswered questions. Neurosci Res 46:127-134.
43. Shoykhet M, Shetty P, Minnery BS, Simons D (2003) Protracted development of responses to whisker deflection in rat trigeminal ganglion neurons. J Neurophysiol 90:1432-1437.
44. Single FN, Rozov A, Burnashev N, Zimmermann F, Hanley DF, Forrest D, Curan T, Jensen V, Hvalby O, Sprengel R, Seeburg PH (2000) Dysfunctions in mice by NMDA receptor point mutations NR1(N598Q) and NR1(N598R). J Neurosci 20:2558-2566.
45. Sugimoto T, Xiao C, Takeyama A, He Y-F, Takano-Yamamoto T, Ichikawa H (1999) Apoptotic cascade of neurons in the subcortical sensory relay nuclei following the neonatal infraorbital nerve transection. Brain Res 824:284-290.
46. Triller A, Choquet D (2005) Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28:133-139.
47. Waite PM, Li L, Ashwell KW (1992) Developmental and lesion induced cell death in the rat ventrobasal complex. NeuroReport 3:485-488.
48. Woolsey TA (1990) Peripheral alteration and somatosensory development. In: Development of Sensory Systems in Mammals (Coleman EJ, ed), pp 461-516. New York: Wiley.
49. Zhang LI, Tao HW, Poo M-M (2000) Visual input induces long-term potentiation of developing retinotectal synapses. Nat Neurosci 3:708-715.
50. Zheng X, Zhang L, Wang AP, Araneda RC, Lin Y, Zukin RS, Bennett MVL (1999) Mutation of structural determinants lining the N-methyl-D-aspartate receptor channel differentially affects phencyclidine block and spermine potentiation and block. Neuroscience 93:125-134.
51. Zhou Q, Tao H-W, Poo M-M (2003) Reversal and stabilization of synaptic modifications in a developing visual system. Science 300:1953-1957.