Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus

Cerebral Cortex

Volumn 20, Issue 11, 2010, Pages 2712-2727

  Morellini, Fabio ^a   Sivukhina, Elena ^a   Stoenica, Luminita ^a   Oulianova, Elena ^a   Bukalo, Olena ^a   Jakovcevski, Igor ^a   Dityatev, Alexander ^a,b   Irintchev, Andrey ^a,c   Schachner, Melitta ^a,d,e  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d RUTGERS UNIVERSITY   (United States)

^e SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

behavior; electrophysiology; hippocampus; inhibition; morphology

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; PARVALBUMIN; TENASCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CONTROLLED STUDY; DENTATE GYRUS; GABAERGIC TRANSMISSION; GRANULE CELL; INTERNEURON; LEARNING; MALE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; WORKING MEMORY;

ANIMALS; COGNITION; DENTATE GYRUS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; LEARNING; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; TENASCIN;

EID: 77954514610     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq017     Document Type: Article

References (54)

1. Abdul-Monim Z, Neill JC, Reynolds GP. 2007. Sub-chronic psychotomi-metic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat. J Psychopharmacol. 21:198-205.
2. Bampton ET, Gray RA, Large CH. 1999. Electrophysiological characterisation of the dentate gyrus in five inbred strains of mouse. Brain Res. 841:123-134.
3. Barnard EA, Skolnick P, Olsen RW, Mohler H, Diehard W, Baggie G, Bastrop C, Bateson AN, Langer SZ. 1998. International union of pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev. 50:291-313.
4. Berghuis P, Dobszay MB, Sousa KM, Schulte G, Mager PP, Hartig W, Gorcs TJ, Zilberter Y, Ernfors P, Harkany T. 2004. Brain-derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fast-spiking GABAergic interneurons. Eur J Neurosci. 20:1290-1306.
5. Brandewiede J, Schachner M, Morellini F. 2005. Ethological analysis of the senescence-accelerated P/8 mouse. Behav Brain Res. 158:109-121.
6. Bukalo O, Schachner M, Dityatev A. 2007. Hippocampal metaplasticity induced by deficiency in the extracellular matrix glycoprotein tenascin-R. J Neurosci. 27:6019-6028.
7. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, et al. 2000. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature. 408:975-979.
8. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. 378:75-78.
9. Davis S, Bliss TV, Dutrieux G, Laroche S, Errington ML. 1997. Induction and duration of long-term potentiation in the hippocampus of the freely moving mouse. J Neurosci Methods. 75:75-80.
10. Errington ML, Bliss TV, Morris RJ, Laroche S, Davis S. 1997. Long-term potentiation in awake mutant mice. Nature. 387:666-667.
11. Fabricius K, Wortwein G, Pakkenberg B. 2008. The impact of maternal separation on adult mouse behavior and on the total neuron number in the mouse hippocampus. Brain Struct Funct. 212:403-416.
12. Fellini L, Schachner M, Morellini F. 2006. Adult but not aged C57BL/6 male mice are capable of using geometry for orientation. Learn Mem. 13:473-481.
13. Freitag S, Schachner M, Morellini F. 2003. Behavioral alterations in mice deficient for the extracellular matrix glycoprotein tenascin-R. Behav Brain Res. 145:189-207.
14. Freund TF. 2003. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 26:489-495.
15. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus. 6:347-470.
16. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN, et al. 2007. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron. 53:591-604.
17. Fuss B, Wintergerst ES, Bartsch U, Schachner M. 1993. Molecular characterization and in situ mRNA localization of the neural recognition molecule J1-160/180: a modular structure similar to tenascin. J Cell Biol. 120:1237-1249.
18. Hanse E, Gustafsson B. 1992. Long-term potentiation and field EPSPs in the lateral and medial perforant paths in the dentate gyrus in vitro: a comparison. Eur J Neurosci. 4:1191-1201.
19. Hartig W, Brauer K, Bruckner G. 1992. Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport. 3:869-872.
20. Hernandez-Rabaza V, Barcia JA, Llorens-Martin M, Trejo JL, Canales JJ. 2007. Spared place and object-place learning but limited spatial working memory capacity in rats with selective lesions of the dentate gyrus. Brain Res Bull. 72:315-323.
21. Hsu D. 2007. The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res. 163:601-613.
22. Irintchev A, Rollenhagen A, Troncoso E, Kiss JZ, Schachner M. 2005. Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb Cortex. 15:950-962.
23. Jung MW, McNaughton BL. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus. 3:165-182.
24. LeeI,Kesner RP. 2004. Encoding versus retrievalofspatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus. 14:66-76.
25. Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 6:312-324.
26. Liao H, Huang W, Schachner M, Guan Y, Guo J, Yan J, Qin J, Bai X, Zhang L. 2008. Beta 1 integrin mediated effects of tenascin-R domains EGFL and FN6-8 on neural stem/progenitor cell proliferation and differentiation in vitro. J Biol Chem. 283:27927-27936.
27. Long JM, Kalehua AN, Muth NJ, Hengemihle JM, Jucker M, Calhoun ME, Ingram DK, Mouton PR. 1998. Stereological estimation of total microglia number in mouse hippocampus. J Neurosci Methods. 84:101-108. (Pubitemid 28485053)
28. Madden SD, Donovan M, Cotter TG. 2007. Key apoptosis regulating proteins are down-regulated during postnatal tissue development. Int J Dev Biol. 51:415-423.
29. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat Rev Neurosci. 2:11-23.
30. McHugh TJ, Jones MW, Quinn JJ, Balthasarm N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science. 317:94-99.
31. Mitchell SJ, Silver RA. 2003. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron. 38:433-445.
32. Montag-Sallaz M, Montag D. 2003. Severe cognitive and motor coordination deficits in tenascin-R-deficient mice. Genes Brain Behav. 2:20-31.
33. Morellini F, Schachner M. 2006. Enhanced novelty-induced activity, reduced anxiety, delayed resynchronization to daylight reversal and weaker muscle strength in tenascin-C-deficient mice. Eur J Neuro-sci. 23:1255-1268.
34. Morganti MC, Taylor J, Pesheva P, Schachner M. 1990. Oligodendrocyte- derived J1-160/180 extracellular matrix glycoproteins are adhesive or repulsive depending on the partner cell type and time of interaction. Exp Neurol. 109:98-110.
35. Morris RG, Frey U. 1997. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B Biol Sci. 352:1489-1503.
36. Neill JC, Sarkisian MR, Wang Y, Liu Z, Yu L, Tandon P, Zhang G, Holmes GL, Geller AI. 2001. Enhanced auditory reversal learning by genetic activation of protein kinase C in small groups of rat hippocampal neurons. Brain Res Mol Brain Res. 93:127-136.
37. Niewoehner B, Single FN, Hvalby O, Jensen V, Borgloh SM, Seeburg PH, Rawlins JN, Sprengel R, Bannerman DM. 2007. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur J Neurosci. 25:837-846.
38. Nikonenko A, Schmidt S, Skibo G, Bruckner G, Schachner M. 2003. Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J Comp Neurol. 456:338-349.
39. Nikonenko AG, Sun M, Lepsveridze E, Apostolova I, Petrova I, Irintchev A, Dityatev A, Schachner M. 2006. Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. Eur J Neurosci. 23:1839-1852.
40. Nosten-Bertrand M, Errington ML, Murphy KP, Tokugawa Y, Barboni E, Kozlova E, Michalovich D, Morris RG, Silver J, Stewart CL, et al. 1996. Normal spatial learning despite regional inhibition of LTP in mice lacking Thy-1. Nature. 379:826-829.
41. Okada T, Yamada N, Tsuzuki K, Horikawa HP, Tanaka K, Ozawa S. 2003. Long-term potentiation in the hippocampal CA1 area and dentate gyrus plays different roles in spatial learning. Eur J Neurosci. 17:341-349.
42. Reznikov KY. 1991. Cell proliferation and cytogenesis in the mouse hippocampus. Adv Anat Embryol Cell Biol. 122:1-74.
43. Ribak CE, Shapiro LA. 2007. Ultrastructure and synaptic connectivity of cell types in the adult rat dentate gyrus. Prog Brain Res. 163:155-166.
44. Rolls ET, Kesner RP. 2006. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol. 79:1-48.
45. Snyder JS, Kee N, Wojtowicz JM. 2001. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol. 85:2423-2431. (Pubitemid 32525520)
46. Stoenica L, Senkov O, Gerardy-Schahn R, Weinhold B, Schachner M, Dityatev A. 2006. In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. Eur J Neurosci. 23:2255-2264.
47. Taylor J, Pesheva P, Schachner M. 1993. Influence of janusin and tenascin on growth cone behavior in vitro. J Neurosci Res. 35:347-362.
48. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, et al. 1999. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci. 19:4245-4262.
49. Wei W, Zhang N, Peng Z, Houser CR, Mody I. 2003. Perisynaptic localization of delta subunit-containing GABAA receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci. 23:10650-10661.
50. Wintergerst ES, Fuss B, Bartsch U. 1993. Localization of janusin mRNA in the central nervous system of the developing and adult mouse. Eur J Neurosci. 5:299-310.
51. Woo NH, Lu B. 2006. Regulation of cortical interneurons by neuro-trophins: from development to cognitive disorders. Neuroscientist. 12:43-56.
52. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. 2000. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron. 27:623-633.
53. Woodworth A, Fiete D, Baenziger JU. 2002. Spatial and temporal regulation of tenascin-R glycosylation in the cerebellum. J Biol Chem. 277:50941-50947.
54. Xavier GF, Oliveira-Filho FJ, Santos AM. 1999. Dentate gyrus-selective colchicine lesion and disruption of performance in spatial tasks: difficulties in "place strategy" because of a lack of flexibility in the use of environmental cues? Hippocampus. 9: 668-681.