Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of down syndrome

Journal of Neuroscience

Volumn 24, Issue 37, 2004, Pages 8153-8160

  Kleschevnicov, Alexander M ^a   Belichenko, Pavel V ^a   Villar, Angela J ^c   Epstein, Charles J ^c   Malenka, Robert C ^b   Mobley, William C ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dentate; Down syndrome; GABAergic; Gyrus; Inhibition; Long term potentiation; Presynaptic; Synaptic

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PICROTOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME 21; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DOWN SYNDROME; HIPPOCAMPUS; LEARNING DISORDER; LONG TERM POTENTIATION; MEMORY DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; COGNITION DISORDERS; CROSSES, GENETIC; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; EVOKED POTENTIALS; FEMALE; GENE DOSAGE; GLYCINE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MAGNESIUM; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PRESYNAPTIC TERMINALS; QUINOXALINES; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SPECIES SPECIFICITY; TRISOMY;

EID: 4644250821     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1766-04.2004     Document Type: Article

References (57)

1. Adamec RE, McNaughton B, Racine R, Livingston KE (1981) Effects of diazepam on hippocampal excitability in the rat: action in the dentate area. Epilepsia 22:205-215.
2. Antonarakis SE, Lyle R, Chrast R, Scott HS (2001) Differential gene expression studies to explore the molecular pathophysiology of Down syndrome. Brain Res Brain Res Rev 36:265-274.
3. Auld DS, Kar S, Quirion R (1998) Beta-amyloid peptides as direct cholinergic neuromodulators: a missing link? Trends Neurosci 21:43-49.
4. Aylward EH, Li Q, Honeycutt NA, Warren AC, Pulsifer MB, Barta PE, Chan MD, Smith PD, Jerram M, Pearlson GD (1999) MRI volumes of the hippocampus and amygdala in adults with Down's syndrome with and without dementia. Am J Psychiatry 156:564-568.
5. Barnes CA (1979) Memory deficits associated with senescence: a neuro-physiological and behavioral study in the rat. J Comp Physiol Psychol 93:74-104.
6. Bayazitov I, Kleschevnikov A (2000) Afferent high strength tetanizations favour potentiation of the NMDA vs. AMPA receptor-mediated component of field EPSP in CA1 hippocampal slices of rats. Brain Res 866:188-196.
7. Bilkey DK, Goddard GV (1985) Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones. Brain Res 361:99-106.
8. Carlesimo GA, Marotta L, Vicari S (1997) Long-term memory in mental retardation: evidence for a specific impairment in subjects with Down's syndrome. Neuropsychologia 35:71-79.
9. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
10. Chapman RS, Hesketh LJ (2000) Behavioral phenotype of individuals with Down syndrome. Ment Retard Dev Disabil Res Rev 6:84-95.
11. Cooper JD, Salehi A, Delcroix JD, Howe CL, Belichenko PV, Chua-Couzens J, Kilbridge JF, Carlson EJ, Epstein CJ, Mobley WC (2001) Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc Natl Acad Sci USA 98:10439-10444.
12. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470-478.
13. Cullen WK, Suh YH, Anwyl R, Rowan MJ (1997) Block of LTP in rat hippocampus in vivo by beta-amyloid precursor protein fragments. Neuro-Report 8:3213-3217.
14. Davisson MT, Schmidt C, Akeson EC (1990) Segmental trisomy of murine chromosome 16: a new model system for studying Down syndrome. Prog Clin Biol Res 360:263-280.
15. Davisson MT, Schmidt C, Reeves RH, Irving NG, Akeson EC, Harris BS, Bronson RT (1993) Segmental trisomy as a mouse model for Down syndrome. Prog Clin Biol Res 384:117-133.
16. Demas GE, Nelson RJ, Krueger BK, Yarowsky PJ (1996) Spatial memory deficits in segmental trisomic Ts65Dn mice. Behav Brain Res 82:85-92.
17. Demas GE, Nelson RJ, Krueger BK, Yarowsky PJ (1998) Impaired spatial working and reference memory in segmental trisomy (Ts65Dn) mice. Behav Brain Res 90:199-201.
18. Dewachter I, van Dorpe J, Spittaels K, Tesseur I, Van Den Haute C, Moechars D, Van Leuven F (2000) Modeling Alzheimer's disease in transgenic mice: effect of age and of presenilin1 on amyloid biochemistry and pathology in APP/London mice. Exp Gerontol 35:831-841.
19. Dierssen M, Fillat C, Crnic L, Arbones M, Florez J, Estivill X (2001) Murine models for Down syndrome. Physiol Behav 73:859-871.
20. Engel Jr J (1996) Excitation and inhibition in epilepsy. Can J Neurol Sci 23:167-174.
21. Epstein CJ (2002) 2001 William Allan Award Address. From Down syndrome to the "human" in "human genetics." Am J Hum Genet 70:300-313.
22. Escorihuela RM, Vallina IF, Martinez-Cue C, Baamonde C, Dierssen M, Tobena A, Florez J, Fernandez-Teruel A (1998) Impaired short-and long-term memory in Ts65Dn mice, a model for Down syndrome. Neurosci Lett 247:171-174.
23. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479-486.
24. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
25. Galdzicki Z, Siarey R, Pearce R, Stoll J, Rapoport SI (2001) On the cause of mental retardation in Down syndrome: extrapolation from full and segmental trisomy 16 mouse models. Brain Res Brain Res Rev 35:115-145.
26. Gardiner K, Fortna A, Bechtel L, Davisson MT (2003) Mouse models of Down syndrome: how useful can they be? Comparison of the gene content of human chromosome 21 with orthologous mouse genomic regions. Gene 318:137-147.
27. Hill JM, Ades AM, McCune SK, Sahir N, Moody EM, Abebe DT, Crnic LS, Brenneman DE (2003) Vasoactive intestinal peptide in the brain of a mouse model for Down syndrome. Exp Neurol 183:56-65.
28. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen K, Sun Y, Carlson E (1996) Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci USA 93:13333-13338.
29. Hunter CL, Bimonte HA, Granholm AC (2003) Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age-related impairments in working and reference memory. Behav Brain Res 138:121-131.
30. Hyde LA, Crnic LS (2001) Age-related deficits in context discrimination learning in Ts65Dn mice that model Down syndrome and Alzheimer's disease. Behav Neurosci 115:1239-1246.
31. Hyde LA, Frisone DF, Crnic LS (2001) Ts65Dn mice, a model for Down syndrome, have deficits in context discrimination learning suggesting impaired hippocampal function. Behav Brain Res 118:53-60.
32. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R (2003) APP processing and synaptic function. Neuron 37:925-937.
33. Korenberg JR, Chen XN, Schipper R, Sun Z, Gonsky R, Gerwehr S, Carpenter N, Daumer C, Dignan P, Disteche C (1994) Down syndrome phenotypes: the consequences of chromosomal imbalance. Proc Natl Acad Sci USA 91:4997-5001.
34. Krasuski JS, Alexander GE, Horwitz B, Rapoport SI, Schapiro MB (2002) Relation of medial temporal lobe volumes to age and memory function in nondemented adults with Down's syndrome: implications for the prodromal phase of Alzheimer's disease. Am J Psychiatry 159:74-81.
35. Kurt MA, Davies DC, Kidd M, Dierssen M, Florez J (2000) Synaptic deficit in the temporal cortex of partial trisomy 16 (Ts65Dn) mice. Brain Res 858:191-197.
36. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
37. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C (2003) Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.
38. Moyer Jr JR, Brown TH (1998) Methods for whole-cell recording from visually preselected neurons of perirhinal cortex in brain slices from young and aging rats. J Neurosci Methods 86:35-54.
39. O'Bryan JP, Mohney RP, Oldham CE (2001) Mitogenesis and endocytosis: what's at the INTERSECTIoN? Oncogene 20:6300-6308.
40. Paternain AV, Herrera MT, Nieto MA, Lerma J (2000) GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20:196-205.
41. Pennington BF, Moon J, Edgin J, Stedron J, Nadel L (2003) The neuropsychology of Down syndrome: evidence for hippocampal dysfunction. Child Dev 74:75-93.
42. Pinter JD, Brown WE, Eliez S, Schmitt JE, Capone GT, Reiss AL (2001) Amygdala and hippocampal volumes in children with Down syndrome: a high-resolution MRI study. Neurology 56:972-974.
43. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, Schmidt C, Bronson RT, Davisson MT (1995) A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 11:177-184.
44. Reeves RH, Baxter LL, Richtsmeier JT (2001) Too much of a good thing: mechanisms of gene action in Down syndrome. Trends Genet 17:83-88.
45. Roizen NJ, Patterson D (2003) Down's syndrome. Lancet 361:1281-1289.
46. Saal D, Dong Y, Bonci A, Malenka RC (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577-582.
47. Sago H, Carlson EJ, Smith DJ, Rubin EM, Crnic LS, Huang TT, Epstein CJ (2000) Genetic dissection of region associated with behavioral abnormalities in mouse models for Down syndrome. Pediatr Res 48:606-613.
48. Schafer DA (2002) Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol 14:76-81.
49. Siarey RJ, Stoll J, Rapoport SI, Galdzicki Z (1997) Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down syndrome. Neuropharmacology 36:1549-1554.
50. Siarey RJ, Carlson EJ, Epstein CJ, Balbo A, Rapoport SI, Galdzicki Z (1999) Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down syndrome. Neuropharmacology 38:1917-1920.
51. Slepnev VI, De Camilli P (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 1:161-172.
52. Stafstrom CE (1993) Epilepsy in Down syndrome: clinical aspects and possible mechanisms. Am J Ment Retard 98:12-26.
53. Swanson TH, Sperling MR, O'Connor MJ (1998) Strong paired pulse depression of dentate granule cells in slices from patients with temporal lobe epilepsy. J Neural Transm 105:613-625.
54. Sylvester PE (1983) The hippocampus in Down's syndrome. J Ment Defic Res 27:227-236.
55. Vicari S, Bellucci S, Carlesimo GA (2000) Implicit and explicit memory: a functional dissociation in persons with Down syndrome. Neuropsychologia 38:240-251.
56. Wisniewski KE, Wisniewski HM, Wen GY (1985) Occurrence of neuropathological changes and dementia of Aizheimer's disease in Down's syndrome. Ann Neurol 17:278-282.
57. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.