Unilateral entorhinal denervation leads to long-lasting dendritic alterations of mouse hippocampal granule cells

Experimental Neurology

Volumn 230, Issue 2, 2011, Pages 176-185

  Vuksic, Mario ^a,b   Del Turco, Domenico ^a   Vlachos, Andreas ^a   Schuldt, Gerlind ^a   Müller, Christian M ^a,c   Schneider, Gaby ^a   Deller, Thomas ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Dendritic spine; Dentate gyrus; Entorhinal cortex lesion; Regeneration; Sprouting

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATROPHY; BRAIN CORTEX LESION; CELL DENSITY; CELL SIZE; CELL SURVIVAL; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; DENERVATION; ENTORHINAL CORTEX; GRANULE CELL; HIPPOCAMPUS; MALE; MOUSE; NERVE REGENERATION; NERVE SPROUTING; NERVE TRANSECTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REINNERVATION; SENSORY NERVE; THREE DIMENSIONAL IMAGING;

ACETYLCHOLINESTERASE; ANIMALS; DENDRITES; DENERVATION; ENTORHINAL CORTEX; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; NEURONS; PERFORANT PATHWAY; STATISTICS, NONPARAMETRIC;

EID: 79958751339     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.04.011     Document Type: Article

References (53)

1. Bas Orth C., Vlachos A., Del Turco D., Burbach G.J., Haas C.A., Mundel P., Feng G., Frotscher M., Deller T. Lamina-specific distribution of Synaptopodin, an actin-associated molecule essential for the spine apparatus, in identified principal cell dendrites of the mouse hippocampus. J. Comp. Neurol. 2005, 487:227-239.
2. Bas O.C., Schultz C., Muller C.M., Frotscher M., Deller T. Loss of the cisternal organelle in the axon initial segment of cortical neurons in synaptopodin-deficient mice. J. Comp. Neurol. 2007, 504:441-449.
3. Bekkers J.M., Hausser M. Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output. Proc. Natl. Acad. Sci. U. S. A 2007, 104:11447-11452.
4. Blasco-Ibanez J.M., Freund T.F. Distribution, ultrastructure and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 1997, 7:307-320.
5. Brendza R.P., O'Brian C., Simmons K., McKeel D.W., Bales K.R., Paul S.M., Olney J.W., Sanes J.R., Holtzman D.M. PDAPP; YFP double transgenic mice: a tool to study amyloid-ß associated changes in axonal, dendritic, and synaptic structures. J. Comp. Neurol. 2003, 456:375-383.
6. Buhl E.H. Intracellular injection in fixed slices in combination with neuroanatomical tracing techniques and electron microscopy to determine multisynaptic pathways in the brain. Microsc. Res. Tech. 1993, 24:15-30.
7. Caceres A., Steward O. Dendritic reorganization in the denervated dentate gyrus of the rat following entorhinal cortical lesions: a Golgi and electron microscopic analysis. J. Comp. Neurol. 1983, 136:287-295.
8. Copanaki E., Chang S., Vlachos A., Tschape J.A., Muller U.C., Kogel D., Deller T. sAPPalpha antagonizes dendritic degeneration and neuron death triggered by proteasomal stress. Mol. Cell. Neurosci. 2010, 44:386-393.
9. Czarnecki K., Haas C.A., Bas Orth C., Deller T., Frotscher M. Postnatal development of synaptopodin expression in the rodent hippocampus. J. Comp. Neurol. 2005, 490:133-144.
10. Del Turco D., Woods A.G., Gebhardt C., Phinney A.L., Jucker M., Frotscher M., Deller T. Comparison of commissural sprouting in the mouse and rat fascia dentata after entorhinal cortex lesion. Hippocampus 2003, 13:685-699.
11. Deller T., Bas O.C., Vlachos A., Merten T., Del Turco D., Dehn D., Mundel P., Frotscher M. Plasticity of synaptopodin and the spine apparatus organelle in the rat fascia dentata following entorhinal cortex lesion. J. Comp. Neurol. 2006, 499:471-484.
12. Deller T., Del Turco D., Rappert A., Bechmann I. Structural reorganization of the dentate gyrus following entorhinal denervation: species differences between rat and mouse. Prog. Brain Res. 2007, 163:501-528.
13. Deller T., Drakew A., Frotscher M. Different primary target cells are important for fiber lamination in the fascia dentata: a lesson from reeler mutant mice. Exp. Neurol. 1999, 156:239-253.
14. Deller T., Frotscher M. Lesion-induced plasticity of central neurons: sprouting of single fibers in the rat hippocampus after unilateral entorhinal lesion. Prog. Neurobiol. 1997, 53:687-727.
15. Deller T., Frotscher M., Nitsch R. Sprouting of crossed entorhinodentate fibers after a unilateral entorhinal lesion: anterograde tracing of fiber reorganization with phaseolus vulgaris-leucoagglutinin ( PHAL ). J. Comp. Neurol. 1996, 365:42-55.
16. Desmond N.L., Levy W.B. A quantitative anatomical study of the granule cell dendritic fields of the rat dentate gyrus using a novel probabilistic method. J. Comp. Neurol. 1982, 212:131-145.
17. Diekmann S., Ohm T.G., Nitsch R. Long-lasting transneuronal changes in rat dentate granule cell dendrites after entorhinal cortex lesion-a combined intracellular injection and electron microscopy study. Brain Pathol. 1996, 6:205-214.
18. Donohue D.E., Ascoli G.A. A comparative computer simulation of dendritic morphology. PLoS Comput. Biol. 2008, 4:e1000089.
19. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtmann J.W., Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
20. Frotscher M., Heimrich B., Deller T. Sprouting in the hippocampus is layer-specific. Trends Neurosci. 1997, 20:218-223.
21. Goldowitz D., Cotman C.W. Axonal transport and axon sprouting in the adult rat dentate gyrus: an autoradiographic study. Neuroscience 1980, 5:2163-2174.
22. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
23. Jontes J.D., Smith S.J. Filopodia, spines, and the generation of synaptic diversity. Neuron 2000, 27:11-14.
24. Keller-Peck C.R., Walsh M.K., Gan W.B., Feng G., Sanes J.R., Lichtman J.W. Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 2001, 31:381-394.
25. Krestel H.E., Mihaljevic A.L., Hoffman D.A., Schneider A. Neuronal co-expression of EGFP and beta-galactosidase in mice causes neuropathology and premature death. Neurobiol. Dis. 2004, 17:310-318.
26. Liu H.S., Jan M.S., Chou C.K., Chen P.H., Ke N.J. Is green fluorescent protein toxic to the living cells?. Biochem. Biophys. Res. Commun. 1999, 260:712-717.
27. Lynch G., Stanfield B., Cotman C.W. Developmental differences in postlesion axonal growth in the hippocampus. Brain Res. 1973, 59:155-168.
28. Matus A. Growth of dendritic spines: a continuing story. Curr. Opin. Neurobiol. 2005, 15:67-72.
29. Mesulam M.M., Geula C., Moran M.A. Anatomy of cholinesterase inhibition in Alzheimer's disease: effect of physostigmine and tetrahydroaminoacridine on plaques and tangles. Ann. Neurol. 1987, 22:683-691.
30. Muller C.M., Vlachos A., Deller T. Calcium homeostasis of acutely denervated and lesioned dentate gyrus in organotypic entorhino-hippocampal co-cultures. Cell Calcium 2010, 47:242-252.
31. Nadler J.V., Cotman C., Paoletti C., Lynch G.S. Histochemical evidence of altered development of cholinergic fibers in the rat dentate gyrus following lesions. II. Effects of partial entorhinal and simultaneous multiple lesions. J. Comp. Neurol. 1977, 171:589-604.
32. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu. Rev. Physiol. 2002, 64:313-353.
33. Nitsch R., Frotscher M. Maintenance of peripheral dendrites of GABAergic neurons requires specific input. Brain Res. 1991, 554:304-307.
34. Parnavelas J.G., Lynch G., Brecha N., Cotman C.W., Globus A. Spine loss and regrowth in hippocampus following deafferentation. Nature 1974, 248:71-73.
35. Reeves T.M., Steward O. Changes in the firing properties of neurons in the dentate gyrus with denervation and reinnervation: implications for behavioral recovery. Exp. Neurol. 1988, 102:37-49.
36. Schauwecker P.E., McNeill T.H. Dendritic remodeling of dentate granule cells following a combined entorhinal cortex/fimbria fornix lesion. Exp. Neurol. 1996, 141:145-153.
37. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005, 1035:24-31.
38. Segal M. Dendritic spines and long-term plasticity. Nat. Rev. Neurosci. 2005, 6:277-284.
39. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
40. Stanfield B.B., Caviness V.S.J., Cowan W.M. The organization of certain afferents to the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 1979, 185:461-483.
41. Steward O. Reorganization of neuronal circuitry following central nervous system trauma: naturally occurring processes and opportunities for therapeutic intervention 1994, 266-287. The Neurobiology of Central Nervous System Trauma Oxford University Press, New York. S.K. Salzman, A.I. Faden (Eds.).
42. Steward O., Cotman C.W., Lynch G. Growth of a new fiber projection in the brain of adult rats: reinnervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesion. Exp. Brain Res. 1974, 20:45-66.
43. Steward O., Cotman C.W., Lynch G.S. Re-establishment of electrophysiologically functional entorhinal cortical input to the dentate gyrus deafferented by ipsilateral entorhinal lesions: innervation by the contralateral cortex. Exp. Brain Res. 1973, 18:396-414.
44. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
45. van Groen T., Kadish I., Wyss J.M. Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Res. Bull. 2002, 57:553-556.
46. van Groen T., Miettinen P., Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 2003, 13:133-149.
47. Vuksic M., Del Turco D., Bas O.C., Burbach G.J., Feng G., Muller C.M., Schwarzacher S.W., Deller T. 3D-reconstruction and functional properties of GFP-positive and GFP-negative granule cells in the fascia dentata of the Thy1-GFP mouse. Hippocampus 2008, 18:364-375.
48. Weaver C.M., Wearne S.L. Neuronal firing sensitivity to morphologic and active membrane parameters. PLoS Comput. Biol. 2008, 4:e11.
49. West J.R. Age-dependent sprouting in the dentate gyrus demonstrated with anterograde HRP. Brain Res. Bull. 1984, 12:323-330.
50. Williams R.S., Matthysse S. Morphometric analysis of granule cell dendrites in the mouse dentate gyrus. J. Comp. Neurol. 1983, 215:154-164.
51. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 2001, 24:1071-1089.
52. Zimmer J. Extended commissural and ipsilateral projections in postnatally de-entorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 1973, 64:293-311.
53. Zimmer J., Laurberg S., Sunde N. Non-cholinergic afferents determine the distribution of the cholinergic septohippocampal projection: a study of the AChE staining pattern in the rat fascia dentata and hippocampus after lesions, x-irradiation, and intracerebral grafting. Exp. Brain Res. 1986, 64:158-168.