Heightened cortical excitability in aged rodents with memory impairment

Neurobiology of Aging

Volumn 54, Issue , 2017, Pages 144-151

  Haberman, Rebecca P ^a   Koh, Ming Teng ^a   Gallagher, Michela ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Aging; Hippocampal hyperactivity; Levetiracetam; Memory; Parietal cortex; Retrosplenial cortex

Indexed keywords

LEVETIRACETAM; PROTEIN C FOS; ETIRACETAM; PIRACETAM;

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE FUNCTION TEST; CONTROLLED STUDY; CORTICAL EXCITABILITY; DRUG EFFECT; HIPPOCAMPAL CA3 REGION; IN SITU HYBRIDIZATION; MALE; MEMORY DISORDER; NONHUMAN; ORBITAL CORTEX; PARIETAL CORTEX; PHENOTYPE; PROTEIN EXPRESSION; RAT; RETROSPLENIAL CORTEX; RODENT; TASK PERFORMANCE; YOUNG ADULT; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN CORTEX; COGNITION; DISEASE MODEL; LONG EVANS RAT; MEMORY; METABOLISM; PATHOPHYSIOLOGY; PSYCHOLOGY;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CEREBRAL CORTEX; COGNITION; DISEASE MODELS, ANIMAL; MALE; MEMORY; MEMORY DISORDERS; PIRACETAM; PROTO-ONCOGENE PROTEINS C-FOS; RATS, LONG-EVANS;

EID: 85009830749     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.12.021     Document Type: Article

References (49)

1. Andrews-Hanna, J.R., Snyder, A.Z., Vincent, J.L., Lustig, C., Head, D., Raichle, M.E., Buckner, R.L., Disruption of large-scale brain systems in advanced aging. Neuron 56 (2007), 924–935.
2. Bakker, A., Albert, M.S., Krauss, G., Speck, C.L., Gallagher, M., Response of the medial temporal lobe network in amnestic mild cognitive impairment to therapeutic intervention assessed by fMRI and memory task performance. Neuroimage Clin. 7 (2015), 688–698.
3. Bakker, A., Krauss, G.L., Albert, M.S., Speck, C.L., Jones, L.R., Stark, C.E., Yassa, M.A., Bassett, S.S., Shelton, A.L., Gallagher, M., Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74 (2012), 467–474.
4. Bucci, D.J., Rosen, D.L., Gallagher, M., Effects of age on pilocarpine-induced c-fos expression in rat hippocampus and cortex. Neurobiol. Aging 19 (1998), 227–232.
5. Buckner, R.L., Sepulcre, J., Talukdar, T., Krienen, F.M., Liu, H., Hedden, T., Andrews-Hanna, J.R., Sperling, R.A., Johnson, K.A., Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 29 (2009), 1860–1873.
6. Busche, M.A., Chen, X., Henning, H.A., Reichwald, J., Staufenbield, M., Sakmann, B., Konnerth, A., Critical role of soluble amyloid-β for early hippocampal hyperactivity in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 8740–8745.
7. Busche, M.A., Konnerth, A., Neuronal hyperactivity—a key defect in Alzheimer's disease?. Bioessays 37 (2015), 624–632.
8. Curia, G.1, Longo, D., Biagini, G., Jones, R.S., Avoli, M., The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 172 (2008), 143–157.
9. Devi, L., Ohno, M., Effects of levetiracetam, an antiepileptic drug, on memory impairments associated with aging and Alzheimer's disease in mice. Neurobiol. Learn Mem. 102 (2013), 7–11.
10. Dickerson, B.C., Salat, D.H., Greve, D.N., Chua, E.F., Rand-Giovannetti, E., Rentz, D.M., Bertram, L., Mullin, K., Tanzi, R.E., Blacker, D., Albert, M.S., Sperling, R.A., Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65 (2005), 404–411.
11. Drever, B.D., Riedel, G., Platt, B., The cholinergic system and hippocampal plasticity. Behav. Brain Res. 221 (2011), 505–514.
12. Gallagher, M., Burwell, R.D., Relationship of age-related decline across several behavioral domains. Neurobiol. Aging 10 (1989), 691–708.
13. Gallagher, M., Burwell, R., Burchinal, M., Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci. 107 (1993), 618–626.
14. Gallagher, M., Colantuoni, C., Eichenbaum, H., Haberman, R.P., Rapp, P.R., Tanila, H., Wilson, I.A., Individual differences in neurocognitive aging of the medial temporal lobe. Age 28 (2006), 221–233.
15. Gozzi, A., Schwarz, A.J., Large-scale functional connectivity networks in the rodent brain. Neuroimage 127 (2016), 496–509.
16. Haberman, R.P., Colantuoni, C., Koh, M.T., Gallagher, M., Behaviorally activated mRNA expression profiles produce signatures of learning and enhanced inhibition in aged rats with preserved memory. PLoS One, 8, 2013, e83674.
17. Haberman, R.P., Colantuoni, C., Stocker, A.M., Schmidt, A.C., Pedersen, J.T., Gallagher, M., Prominent hippocampal CA3 gene expression profile in neurocognitive aging. Neurobiol. Aging 32 (2011), 1678–1692.
18. Hall, A.M., Throesch, B.T., Buckingham, S.C., Markwardt, S.J., Peng, Y., Wang, Q., Hoffman, D.A., Roberson, E.D., Tau-dependent Kv4.2 depletion and dendritic hyperexcitability in a mouse model of Alzheimer's disease. J. Neurosci. 35 (2015), 6221–6230.
19. Hansen, N.L., Lauritzen, M., Mortensen, E.L., Osler, M., Avlund, K., Fagerlund, B., Rostrup, E., Subclinical cognitive decline in middle-age is associated with reduced task-induced deactivation of the brain's default mode network. Hum. Brain Mapp. 35 (2014), 4488–4498.
20. Hsu, L.M., Liang, X., Gu, H., Brynildsen, J.K., Stark, J.A., Ash, J.A., Lin, C.P., Lu, H., Rapp, P.R., Stein, E.A., Yang, Y., Constituents and functional implications of the rat default mode network. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E4541–E4547.
21. Huijbers, W., Mormino, E.C., Schultz, A.P., Wigman, S., Ward, A.M., Larvie, M., Amariglio, R.E., Marshall, G.A., Rentz, D.M., Johnson, K.A., Sperling, R.A., Amyloid-β deposition in mild cognitive impairment is associated with increased hippocampal activity, atrophy and clinical progression. Brain 138 (2015), 1023–1035.
22. Jones, D.T., Knopman, D.S., Gunter, J.L., Graff-Radford, J., Vemuri, P., Boeve, B.F., Petersen, R.C., Weiner, M.W., Jack, C.R. Jr., Alzheimer's Disease Neuroimaging Initiative. Cascading network failure across the Alzheimer's disease spectrum. Brain 139 (2016), 547–562.
23. Joo, J.Y., Schaukowitch, K., Farbiak, L., Kilaru, G., Kim, T.K., Stimulus-specific combinatorial functionality of neuronal c-fos enhancers. Nat. Neurosci. 19 (2016), 75–83.
24. Koh, M.T., Haberman, R.P., Foti, S., McCown, T.J., Gallagher, M., Treatment strategies targeting excess hippocampal activity benefit aged rats with cognitive impairment. Neuropsychopharmacology 35 (2010), 1016–1025.
25. Koh, M.T., Rosenzweig-Lipson, S., Gallagher, M., Selective GABA(A) α5 positive allosteric modulators improve cognitive function in aged rats with memory impairment. Neuropharmacology 64 (2013), 145–152.
26. Li, J., Martin, S., Tricklebank, M.D., Schwarz, A.J., Gilmour, G., Task-induced modulation of intrinsic functional connectivity networks in the behaving rat. J. Neurosci. 35 (2015), 658–665.
27. Lu, H., Zou, Q., Gu, H., Raichle, M.E., Stein, E.A., Yang, Y., Rat brains also have a default mode network. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 3979–3984.
28. Miller, S.L., Celone, K., DePeau, K., Diamond, E., Dickerson, B.C., Rentz, D., Pihlajamäki, M., Sperling, R.A., Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 2181–2186.
29. Miller, S.L., Fenstermacher, E., Bates, J., Blacker, D., Sperling, R.A., Dickerson, B.C., Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J. Neurol. Neurosurg. Psychiatry 79 (2008), 630–635.
30. Pihlajamäki, M., Sperling, R.A., Functional MRI assessment of task-induced deactivation of the default mode network in Alzheimer's disease and at-risk older individuals. Behav. Neurol. 21 (2009), 77–91.
31. Priel, M.R., Albuquerque, E.X., Short-term effects of pilocarpine on rat hippocampal neurons in culture. Epilepsia 43 (2002), 40–46.
32. Putcha, D., Brickhouse, M., O'Keefe, K., Sullivan, C., Rentz, D., Marshall, G., Dickerson, B., Sperling, R., Hippocampal hyperactivation associated with cortical thinning in Alzheimer's disease signature regions in non-demented elderly adults. J. Neurosci. 31 (2011), 17680–17688.
33. Rapp, P.R., Gallagher, M., Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 9926–9930.
34. Robitsek, J., Ratner, M.H., Stewart, T., Eichenbaum, H., Farb, D.H., Combined administration of levetiracetam and valproic acid attenuates age-related hyperactivity of CA3 place cells, reduces place field area, and increases spatial information content in aged rat hippocampus. Hippocampus 25 (2015), 1541–1555.
35. Robitsek, R.J., Fortin, N.J., Koh, M.T., Gallagher, M., Eichenbaum, H., Cognitive aging: a common decline of episodic recollection and spatial memory in rats. J. Neurosci. 28 (2008), 8945–8954.
36. Sanchez, P.E., Zhu, L., Verret, L., Vossel, K.A., Orr, A.G., Cirrito, J.R., Devidze, N., Ho, K., Yu, G.Q., Palop, J.J., Mucke, L., Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E2895–E2903.
37. Schmid, L.C., Mittag, M., Poll, S., Steffen, J., Wagner, J., Geis, H.R., Schwarz, I., Schmidt, B., Schwarz, M.K., Remy, S., Fuhrmann, M., Dysfunction of somatostatin-positive interneurons associated with memory deficits in an Alzheimer's disease model. Neuron 92 (2016), 1–12.
38. Shi, J.Q., Wang, B.R., Tian, Y.Y., Xu, J., Gao, L., Zhao, S.L., Jiang, T., Xie, H.G., Zhang, Y.D., Antiepileptics topiramate and levetiracetam alleviate behavioral deficits and reduce neuropathology in APPswe/PS1dE9 transgenic mice. CNS Neurosci. Ther. 19 (2013), 871–881.
39. Simkin, D., Hattori, S., Ybarra, N., Musial, T.F., Buss, E.W., Richter, H., Oh, M.M., Nicholson, D.A., Disterhoft, J.F., Aging-related hyperexcitability in CA3 pyramidal neurons is mediated by enhanced a-type K+ channel function and expression. J. Neurosci. 35 (2015), 13206–13218.
40. Sperling, R.A., Laviolette, P.S., O'Keefe, K., O'Brien, J., Rentz, D.M., Pihlajamaki, M., Marshall, G., Hyman, B.T., Selkoe, D.J., Hedden, T., Buckner, R.L., Becker, J.A., Johnson, K.A., Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63 (2009), 178–188.
41. Spiegel, A.M., Koh, M.T., Vogt, N.M., Rapp, P.R., Gallagher, M., Hilar interneuron vulnerability distinguishes aged rats with memory impairment. J. Comp. Neurol. 521 (2013), 3508–3523.
42. Suberbielle, E., Sanchez, P.E., Kravitz, A.V., Wang, X., Ho, K., Eilertson, K., Devidze, N., Kreitzer, A.C., Mucke, L., Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci. 16 (2013), 613–621.
43. Thomé, A., Gray, D.T., Erickson, C.A., Lipa, P., Barnes, C.A., Memory impairment in aged primates is associated with region-specific network dysfunction. Mol. Psychiatry 21 (2016), 1257–1262.
44. Wilson, I.A., Gallagher, M., Eichenbaum, H., Tanila, H., Neurocognitive aging: prior memories hinder new hippocampal encoding. Trends Neurosci. 29 (2006), 662–670.
45. Wilson, I.A., Ikonen, S., Gallagher, M., Eichenbaum, H., Tanila, H., Age-associated alterations of hippocampal place cells are subregion specific. J. Neurosci. 25 (2005), 6877–6886.
46. Wilson, I.A., Ikonen, S., McMahan, R.W., Gallagher, M., Eichenbaum, H., Tanila, H., Place cell rigidity correlates with impaired spatial learning in aged rats. Neurobiol. Aging 24 (2003), 297–305.
47. Yang, S., Megill, A., Ardiles, A.O., Ransom, S., Tran, T., Koh, M.T., Lee, H.K., Gallagher, M., Kirkwood, A., Integrity of mGluR-LTD in the associative/commissural inputs to CA3 correlates with successful aging in rats. J. Neurosci. 33 (2013), 12670–12678.
48. Yassa, M.A., Lacy, J.W., Stark, S.M., Albert, M.S., Gallagher, M., Stark, C.E., Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 21 (2011), 968–979.
49. Yassa, M.A., Stark, S.M., Bakker, A., Albert, M.S., Gallagher, M., Stark, C.E., High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. Neuroimage 51 (2010), 1242–1252.