Expansion and retraction of hippocampal mossy fibers during postweaning development: Strain-specific effects of NMDA receptor blockade

Hippocampus

Volumn 17, Issue 1, 2007, Pages 58-67

  Holahan, Matthew R ^a,b   Honegger, Kyle S ^a   Routtenberg, Aryeh ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

Axons; Pruning; Synaptic dialogue; Synaptophysin; Tau1; Zinc

Indexed keywords

4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MOTILITY; CONTROLLED STUDY; FEMALE; GROWTH REGULATION; HIPPOCAMPUS; LONG EVANS RAT; MALE; NONHUMAN; POSTNATAL DEVELOPMENT; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; STAINING; STRAIN DIFFERENCE; SYMPATHETIC INNERVATION; WEANING; WISTAR RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; INDOLES; MOSSY FIBERS, HIPPOCAMPAL; PIPERAZINES; PREGNANCY; RATS; RATS, LONG-EVANS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SPECIES SPECIFICITY; SYNAPTOPHYSIN; TAU PROTEINS;

EID: 33846866283     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20242     Document Type: Article

References (46)

1. Amaral DG, Dent JA. 1981. Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
2. Bagri A, Cheng HJ, Yaron A, Pleasure SJ, Tessier-Lavigne M. 2003. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113:285-299.
3. Brewer GJ, Cotman CW 1989a. NMDA receptor regulation of neuronal morphology in cultured hippocampal neurons. Neurosci Lett 99:268-273.
4. Brewer GJ, Cotman CW. 1989b. Survival and growth of hippocampal neurons in defined medium at low density: Advantages of a sandwich culture technique or low oxygen. Brain Res 494:65-74.
5. Cameron HA, McEwen BS, Gould E. 1995. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-4692.
6. Cantallops I, Routtenberg A. 1996. Rapid induction by kainic acid of both axonal growth and F1/GAP-43 protein in the adult rat hippocampal granule cells. J Comp Neurol 366:303-319.
7. Cantallops I, Routtenberg; A. 1999. Activity-dependent regulation of axonal growth: Posttranscriptional control of the GAP-43 gene by the NMDA receptor in developing hippocampus. J Neurobiol 41:208-220.
8. Caroni P. 2001. New EMBO members' review: Actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts. EMBO J 20:4332-4336.
9. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E, Pleasure SJ, Lowenstein DH, Skarnes WC, Chedotal A, Tessier-Lavigne M. 2000. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25: 43-56.
10. Cline HT, Constantine-Paton M. 1989. NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3:413-426.
11. Cline HT, Constantine-Paton M. 1990. NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 10: 1197-1216.
12. Cline HT, Debski EA, Constantine-Paton M. 1990. The role of the NMDA receptor in the development of the frog visual system. Adv Exp Med Biol 268:197-203.
13. Cohen-Cory S. 1999. BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo. J Neurosci 19:9996-10003.
14. Colley PA, Routtenberg A. 1993. Long-term potentiation as synaptic dialogue. Brain Res Brain Res Rev 18:115-122.
15. Colonnese MT, Constantine-Paton M. 2006. Developmental period for N-methyl-D-aspartate (NMDA) receptor-dependent synapse elimination correlated with visuotopic map refinement. J Comp Neurol 494:738-751.
16. Colonnese MT, Zhao JP, Constantine-Paton M. 2005. NMDA receptor currents suppress synapse formation on sprouting axons in vivo. J Neurosci 25:1291-1303.
17. Dotti CG, Banker GA, Binder LI. 1987. The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience 23:121-130.
18. Festing MF, Bender K. 1984. Genetic relationships between inbred strains of rats. An analysis based on genetic markers at 28 biochemical loci. Genet Res 44:271-281.
19. Fitzsimonds RM, Poo MM. 1998. Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143-170.
20. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E. 1991. The mossy cells of the fascia dentata: A comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312:145-163.
21. Gaarskjaer FB. 1985. The development of the dentate area and the hippocampal mossy fiber projection of the rat. J Comp Neurol 241:154-170.
22. Gaarskjaer FB. 1986. The organization and development of the hippocampal mossy fiber system. Brain Res 396:335-357.
23. Gao PP, Yue Y, Cerretti DP, Dreyfus C, Zhou R. 1999. Ephrin-dependent growth and pruning of hippocampal axons. Proc Natl Acad Sci U S A 96:4073-4077.
24. Giger RJ, Cloutier JF, Sahay A, Prinjha RK, Levengood DV, Moore SE, Pickering S, Simmons D, Rastan S, Walsh FS, Kolodkin AL, Ginty DD, Geppert M. 2000. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29-41.
25. Holahan MR, Routtenberg A. 2005. Synaptic dialogue: Substrate for protein-synthesis-independent long-term memory. In: Stanton PK, Bramham C, Scharfman HE, editors. Synaptic Plasticity and Transsynaptic Signaling. New York: Springer. pp xiii, 557.
26. Holahan MR, Rekart JL, Sandoval J, Routtenberg A. 2006. Spatial learning induces presynaptic structural remodeling in the hippocampal mossy fiber system of two rat strains. Hippocampus 16:560-570.
27. Kakizawa S, Yamasaki M, Watanabe M, Kano M. 2000. Critical period for activity-dependent synapse elimination in developing cerebellum. J Neurosci 20:4954-4961.
28. Kantor DB, Kolodkin AL. 2003. Curbing the excesses of youth: Moleculax insights into axonal pruning. Neuron 38:849-852.
29. Kempermann G, Jessberger S, Steiner B, Kronenberg G. 2004. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
30. Lipp HP, Schwegler H, Heinuich B, Driscoll P. 1988. Infrapyramidal mossy fibers and two-way avoidance learning: Developmental modification of hippocampal circuitry and adult behavior of rats and mice. J Neurosci 8:1905-1921.
31. Liu XB, Low LK, Jones EG, Cheng HJ. 2005. Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J Neurosci 25:9124-9134.
32. Luo L, O'Leary DD. 2005. Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156.
33. Luo Y, Vallano ML. 1995. Arachidonic acid, but not sodium nitroprusside, stimulates presynaptic protein kinase C, phosphorylation of GAP-43 in rat hippocampal slices and synaptosomes. J Neurochem 64:1808-1818.
34. Luthi A, Schwyzer L, Mateos JM, Gahwiler BH, McKinney RA. 2001. NMDA receptor activation limits the number of synaptic connections during hippocampal development. Nat Neurosci 4:1102-1107.
35. Lynch MA, Clements MP, Voss KL, Bramharn CR, Bliss TV. 1991. Is arachidonic acid a retrograde messenger in long-term potentiation? Biochem Soc Trans 19:391-396.
36. Medina JH, Izquierdo I. 1995. Retrograde messengers, long-term potentiation and memory. Brain Res Brain Res Rev 21:185-194.
37. Nicoll RA, Malenka RC. 1995. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
38. Pearce IA, Cambray-Deakin MA, Burgoyne RD. 1987. Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett 223:143-147.
39. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Mariani J. 1992. Involvement of the N-methyl-D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256:1823-1825.
40. Rabacchi SA, Solowska JM, Kruk B, Luo Y, Raper JA, Baird DH. 1999. Collapsin-1/semaphorin-III/D is regulated developmentally in Purkinje cells and collapses pontocerebellar mossy fiber neuronal growth cones. J Neurosci 19:4437-4448.
41. Ramirez-Amaya V, Balderas I, Sandoval J, Escobar ML, Bermudez-Rattoni F. 2001. Spatial long-term memory is related to mossy fiber synaptogenesis. J Neurosci 21:7340-7348.
42. Rashid NA, Cambray-Deakin MA. 1992. N-Methyl-D-aspartate effects on the growth, morphology and cytoskeleton of individual neurons in vitro. Brain Res Dev Brain Res 67:301-308.
43. Schaechter JD, Benowitz LI. 1993. Activation of protein kinase C by arachidonic acid selectively enhances the phosphorylation of GAP-43 in nerve terminal membranes. J Neurosci 13:4361-4371.
44. Schmidt JT. 2004. Activity-driven sharpening of the retinotectal projection: The search for retrograde synaptic signaling pathways. J Neurobiol 59:114-133.
45. Seress L. 1992. Morphological variability and developmental aspects of monkey and human granule cells: Differences between the rodent and primate dentate gyrus. Epilepsy Res Suppl 7:3-28.
46. Woolley CS, Wenzel HJ, Schwartzkroin PA. 1996. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 373:108-117.