The hippocampus in aging and disease: From plasticity to vulnerability

Neuroscience

Volumn 309, Issue , 2015, Pages 1-16

  Bartsch, T ^a   Wulff, P ^b  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; AMYLOID BETA PROTEIN; ANTINEOPLASTIC AGENT; CALCIUM ION; GLUCOCORTICOID RECEPTOR; GLUTAMATE RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR ANTIBODY; POTASSIUM CHANNEL COMPLEX ANTIBODY; PROSTAGLANDIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ADAPTATION; AGING; ALZHEIMER DISEASE; AMNESIA; ANIMAL BEHAVIOR; ANXIETY; B LYMPHOCYTE; BRAIN DAMAGE; BRAIN ISCHEMIA; CALCIUM HOMEOSTASIS; CALORIC RESTRICTION; CELL FUNCTION; CELL PROLIFERATION; COGNITIVE DEFECT; CYTOKINE PRODUCTION; DEGENERATIVE DISEASE; DENTATE GYRUS; DEPRESSION; DIABETES MELLITUS; DISEASE PREDISPOSITION; EDITORIAL; EMOTION; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; EXERCISE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEAR; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; LYMPHOCYTE PROLIFERATION; MEMBRANE STEADY POTENTIAL; MEMORY CONSOLIDATION; METABOLIC DISORDER; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; NERVE CELL MEMBRANE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE SPROUTING; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARANEOPLASTIC NEUROPATHY; PATHOPHYSIOLOGY; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RADIATION INJURY; SCHIZOPHRENIA; SEIZURE; SLEEP DISORDER; STRESS; SYNAPTIC TRANSMISSION; T LYMPHOCYTE; TEMPORAL LOBE EPILEPSY; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN DISEASE; PHYSIOLOGY;

AGING; ANIMALS; BRAIN DISEASES; HIPPOCAMPUS; HUMANS; NEUROGENESIS; NEURONAL PLASTICITY;

EID: 84945496849     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.07.084     Document Type: Editorial

References (191)

1. Aimone J.B., Li Y., Lee S.W., Clemenson G.D., Deng W., Gage F.H. Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 2014, 94:991-1026.
2. Aksoy-Aksel A., Manahan-Vaughan D. Synaptic strength at the temporoammonic input to the hippocampal CA1 region in vivo is regulated by NMDA receptors, metabotropic glutamate receptors and voltage-gated calcium channels. Neuroscience 2015, 309:191-199.
3. Amaral D.G., Scharfman H.E., Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 2007, 163:3-22.
4. Anderson V.M., Fisniku L.K., Khaleeli Z., Summers M.M., Penny S.A., Altmann D.R., Thompson A.J., Ron M.A., Miller D.H. Hippocampal atrophy in relapsing-remitting and primary progressive MS: a comparative study. Mult Scler 2010, 16:1083-1090.
5. Avignone E., Frenguelli B.G., Irving A.J. Differential responses to NMDA receptor activation in rat hippocampal interneurons and pyramidal cells may underlie enhanced pyramidal cell vulnerability. Eur J Neurosci 2005, 22:3077-3090.
6. Baier P.C., May U., Scheller J., Rose-John S., Schiffelholz T. Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice. Behav Brain Res 2009, 200:192-196.
7. Bakker A., Kirwan C.B., Miller M., Stark C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
8. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 2004, 28:273-283.
9. Barrientos R.M., Frank M.G., Watkins L.R., Maier S.F. Aging-related changes in neuroimmune-endocrine function: implications for hippocampal-dependent cognition. Horm Behav 2012, 62:219-227.
10. Barrientos R.M., Kitt M.M., Watkins L.R., Maier S.F. Neuroinflammation in the normal aging hippocampus. Neuroscience 2015, 309:84-99.
11. Bartsch T. The Clinical Neurobiology of the Hippocampus 2012, Oxford University Press, Oxford, UK.
12. Bartsch T., Alfke K., Stingele R., Rohr A., Freitag-Wolf S., Jansen O., Deuschl G. Selective affection of hippocampal CA-1 neurons in patients with transient global amnesia without long-term sequelae. Brain 2006, 129:2874-2884.
13. Bartsch T., Alfke K., Wolff S., Rohr A., Jansen O., Deuschl G. Focal MR spectroscopy of hippocampal CA-1 lesions in transient global amnesia. Neurology 2008, 70:1030-1035.
14. Bartsch T., Dohring J., Rohr A., Jansen O., Deuschl G. CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness. Proc Natl Acad Sci U S A 2011, 108:17562-17567.
15. Bartsch T., Döhring J., Reuter S., Finke C., Rohr A., Brauer H., Deuschl G., Jansen O. Selective neuronal vulnerability of human hippocampal CA1 neurons: lesion evolution, temporal course, and pattern of hippocampal damage in diffusion-weighted MR imaging. J Cereb Blood Flow Metab 2015, 10.1038/jcbfm.2015.137.
16. Bartsch T., Schonfeld R., Muller F.J., Alfke K., Leplow B., Aldenhoff J., Deuschl G., Koch J.M. Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory. Science 2010, 328:1412-1415.
17. Battaglia F.P., Benchenane K., Sirota A., Pennartz C.M., Wiener S.I. The hippocampus: hub of brain network communication for memory. Trends Cognit Sci 2011, 15:310-318.
18. Bendel O., Bueters T., von Euler M., Ove Ogren S., Sandin J., von Euler G. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J Cereb Blood Flow Metab 2005, 25:1586-1595.
19. Bergmann O., Frisen J. Neuroscience. Why adults need new brain cells. Science 2013, 340:695-696.
20. Bettcher B.M., Gelfand J.M., Irani S.R., Neuhaus J., Forner S., Hess C.P., Geschwind M.D. More than memory impairment in voltage-gated potassium channel complex encephalopathy. Eur J Neurol 2014, 21:1301-1310.
21. Bien C.G., Urbach H., Schramm J., Soeder B.M., Becker A.J., Voltz R., Vincent A., Elger C.E. Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy. Neurology 2007, 69:1236-1244.
22. Bliss T., Schoepfer R. Neuroscience. Controlling the ups and downs of synaptic strength. Science 2004, 304:973-974.
23. Blümcke I, Coras R (2015) Clinico-pathological subtypes of hippocampal sclerosis in temporal lobe epilepsy and their differential impact on memory impairment. Neuroscience 309:153-161.
24. Bonnici H.M., Chadwick M.J., Kumaran D., Hassabis D., Weiskopf N., Maguire E.A. Multi-voxel pattern analysis in human hippocampal subfields. Front Hum Neurosci 2012, 6:290.
25. Bonnici H.M., Chadwick M.J., Maguire E.A. Representations of recent and remote autobiographical memories in hippocampal subfields. Hippocampus 2013, 23:849-854.
26. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 1995, 16:271-278. Discussion 278-284.
27. Braak H., Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol Scand Suppl 1996, 165:3-12.
28. Brainin M., Goldenberg G., Ahlers C., Reisner T., Neuhold A., Deecke L. Structural brain correlates of anterograde memory deficits in multiple sclerosis. J Neurol 1988, 235:362-365.
29. Braun O., Dewitz C., Moller-Hackbarth K., Scheller J., Schiffelholz T., Baier P.C., Rose-John S. Effects of blockade of peripheral interleukin-6 trans-signaling on hippocampus-dependent and independent memory in mice. J Interferon Cytokine Res 2013, 33:254-260.
30. Brown J., Cooper-Kuhn C.M., Kempermann G., Van Praag H., Winkler J., Gage F.H., Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003, 17:2042-2046.
31. Bueters T., von Euler M., Bendel O., von Euler G. Degeneration of newly formed CA1 neurons following global ischemia in the rat. Exp Neurol 2008, 209:114-124.
32. Burger C. Region-specific genetic alterations in the aging hippocampus: implications for cognitive aging. Front Aging Neurosci 2010, 2:140.
33. Burke S.N., Barnes C.A. Neural plasticity in the ageing brain. Nat Rev Neurosci 2006, 7:30-40.
34. Burke S.N., Barnes C.A. Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 2010, 33:153-161.
35. Butler T.R., Self R.L., Smith K.J., Sharrett-Field L.J., Berry J.N., Littleton J.M., Pauly J.R., Mulholland P.J., Prendergast M.A. Selective vulnerability of hippocampal cornu ammonis 1 pyramidal cells to excitotoxic insult is associated with the expression of polyamine-sensitive N-methyl-d-asparate-type glutamate receptors. Neuroscience 2010, 165:525-534.
36. Buzsaki G., Moser E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 2013, 16:130-138.
37. Carpentier P.A., Palmer T.D. Immune influence on adult neural stem cell regulation and function. Neuron 2009, 64:79-92.
38. Cendes F., Sakamoto A.C., Spreafico R., Bingaman W., Becker A.J. Epilepsies associated with hippocampal sclerosis. Acta Neuropathol 2014, 128:21-37.
39. Chen P.E., Errington M.L., Kneussel M., Chen G., Annala A.J., Rudhard Y.H., Rast G.F., Specht C.G., Tigaret C.M., Nassar M.A., Morris R.G., Bliss T.V., Schoepfer R. Behavioral deficits and subregion-specific suppression of LTP in mice expressing a population of mutant NMDA receptors throughout the hippocampus. Learn Mem 2009, 16:635-644.
40. Chetelat G., Fouquet M., Kalpouzos G., Denghien I., De la Sayette V., Viader F., Mezenge F., Landeau B., Baron J.C., Eustache F., Desgranges B. Three-dimensional surface mapping of hippocampal atrophy progression from MCI to AD and over normal aging as assessed using voxel-based morphometry. Neuropsychologia 2008, 46:1721-1731.
41. Coultrap S.J., Nixon K.M., Alvestad R.M., Valenzuela C.F., Browning M.D. Differential expression of NMDA receptor subunits and splice variants among the CA1, CA3 and dentate gyrus of the adult rat. Brain Res Mol Brain Res 2005, 135:104-111.
42. Cramer S.C., Sur M., Dobkin B.H., O'Brien C., Sanger T.D., Trojanowski J.Q., Rumsey J.M., Hicks R., Cameron J., Chen D., Chen W.G., Cohen L.G., deCharms C., Duffy C.J., Eden G.F., Fetz E.E., Filart R., Freund M., Grant S.J., Haber S., Kalivas P.W., Kolb B., Kramer A.F., Lynch M., Mayberg H.S., McQuillen P.S., Nitkin R., Pascual-Leone A., Reuter-Lorenz P., Schiff N., Sharma A., Shekim L., Stryker M., Sullivan E.V., Vinogradov S. Harnessing neuroplasticity for clinical applications. Brain 2011, 134:1591-1609.
43. Czepiel M., Boddeke E., Copray S. Human oligodendrocytes in remyelination research. Glia 2015, 63:513-530.
44. Das S.R., Avants B.B., Pluta J., Wang H., Suh J.W., Weiner M.W., Mueller S.G., Yushkevich P.A. Measuring longitudinal change in the hippocampal formation from in vivo high-resolution T2-weighted MRI. Neuroimage 2012, 60:1266-1279.
45. de Flores R, La Joie R, Chétetat G (2015a) Structural imaging of hippocampal subfields in healthy aging and Alzheimer's disease. Neuroscience 309:29-50.
46. de Flores R., La Joie R., Landeau B., Perrotin A., Mezenge F., de La Sayette V., Eustache F., Desgranges B., Chetelat G. Effects of age and Alzheimer's disease on hippocampal subfields: comparison between manual and FreeSurfer volumetry. Hum Brain Mapp 2015, 36:463-474.
47. de Kloet E.R., Joels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005, 6:463-475.
48. de Kloet R (2012) Stress and the Hippocampus. In: The clinical neurobiology of the hippocampus (Th. Bartsch, ed), pp 77-104. Oxford: Oxford University Press.
49. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
50. Deuker L., Doeller C.F., Fell J., Axmacher N. Human neuroimaging studies on the hippocampal CA3 region - integrating evidence for pattern separation and completion. Front Cell Neurosci 2014, 8:64.
51. Diekelmann S., Born J. The memory function of sleep. Nat Rev Neurosci 2010, 11:114-126.
52. Dietrich J., Prust M., Kaiser J. Chemotherapy, cognitive impairment and hippocampal toxicity. Neuroscience 2015, 309:224-232.
53. Dohring J., Schmuck A., Bartsch T. Stress-related factors in the emergence of transient global amnesia with hippocampal lesions. Front Behav Neurosci 2014, 8:287.
54. Dong H.W., Swanson L.W., Chen L., Fanselow M.S., Toga A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci U S A 2009, 106:11794-11799.
55. Drapeau E., Mayo W., Aurousseau C., Le Moal M., Piazza P.V., Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A 2003, 100:14385-14390.
56. Dutta R., Chang A., Doud M.K., Kidd G.J., Ribuado M.V., Young E.A., Fox R.J., Staugaitis S.M., Trapp B.D. Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Ann Neurol 2011, 69:445-454.
57. Dutta R., Chomyk A.M., Chang A., Ribaudo M.V., Deckard S.A., Doud M.K., Edberg D.D., Bai B., Li M., Baranzini S.E., Fox R.J., Staugaitis S.M., Macklin W.B., Trapp B.D. Hippocampal demyelination and memory dysfunction are associated with increased levels of the neuronal microRNA miR-124 and reduced AMPA receptors. Ann Neurol 2013, 73:637-645.
58. Engvig A., Fjell A.M., Westlye L.T., Skaane N.V., Sundseth O., Walhovd K.B. Hippocampal subfield volumes correlate with memory training benefit in subjective memory impairment. Neuroimage 2012, 61:188-194.
59. Erion J.R., Wosiski-Kuhn M., Dey A., Hao S., Davis C.L., Pollock N.K., Stranahan A.M. Obesity elicits interleukin 1-mediated deficits in hippocampal synaptic plasticity. J Neurosci 2014, 34:2618-2631.
60. Falkai P, Gruber O, Schmitt A (2012) Schizophrenia. In: The clinical neurobiology of the hippocampus (Th. Bartsch, ed). Oxford: Oxford University Press.
61. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
62. Finke C., Bruehl H., Duzel E., Heekeren H.R., Ploner C.J. Neural correlates of short-term memory reorganization in humans with hippocampal damage. J Neurosci 2013, 33:11061-11069.
63. Finke C., Kopp U.A., Scheel M., Pech L.M., Soemmer C., Schlichting J., Leypoldt F., Brandt A.U., Wuerfel J., Probst C., Ploner C.J., Pruss H., Paul F. Functional and structural brain changes in anti-N-methyl-D-aspartate receptor encephalitis. Ann Neurol 2013, 74:284-296.
64. Fontan-Lozano A., Saez-Cassanelli J.L., Inda M.C., de los Santos-Arteaga M., Sierra-Dominguez S.A., Lopez-Lluch G., Delgado-Garcia J.M., Carrion A.M. Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. J Neurosci 2007, 27:10185-10195.
65. Forster A., Griebe M., Gass A., Kern R., Hennerici M.G., Szabo K. Diffusion-weighted imaging for the differential diagnosis of disorders affecting the hippocampus. Cerebrovasc Dis 2012, 33:104-115.
66. Fotuhi M., Do D., Jack C. Modifiable factors that alter the size of the hippocampus with ageing. Nat Rev Neurol 2012, 8:189-202.
67. Fouquet M., Desgranges B., La Joie R., Riviere D., Mangin J.F., Landeau B., Mezenge F., Pelerin A., de La Sayette V., Viader F., Baron J.C., Eustache F., Chetelat G. Role of hippocampal CA1 atrophy in memory encoding deficits in amnestic mild cognitive impairment. Neuroimage 2012, 59:3309-3315.
68. Freund J., Brandmaier A.M., Lewejohann L., Kirste I., Kritzler M., Kruger A., Sachser N., Lindenberger U., Kempermann G. Emergence of individuality in genetically identical mice. Science 2013, 340:756-759.
69. Gee C.E., Benquet P., Raineteau O., Rietschin L., Kirbach S.W., Gerber U. NMDA receptors and the differential ischemic vulnerability of hippocampal neurons. Eur J Neurosci 2006, 23:2595-2603.
70. Geurts J.J., Bo L., Roosendaal S.D., Hazes T., Daniels R., Barkhof F., Witter M.P., Huitinga I., van der Valk P. Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 2007, 66:819-827.
71. Gold S.M., Kern K.C., O'Connor M.F., Montag M.J., Kim A., Yoo Y.S., Giesser B.S., Sicotte N.L. Smaller cornu ammonis 2-3/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms. Biol Psychiatry 2010, 68:553-559.
72. Gold S.M., O'Connor M.F., Gill R., Kern K.C., Shi Y., Henry R.G., Pelletier D., Mohr D.C., Sicotte N.L. Detection of altered hippocampal morphology in multiple sclerosis-associated depression using automated surface mesh modeling. Hum Brain Mapp 2014, 35:30-37.
73. Gray DT, Barnes CA (2015) Distinguishing adaptive plasticity from vulnerability in the aging hippocampus. Neuroscience 309:17-28.
74. Guzowski J.F., Knierim J.J., Moser E.I. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 2004, 44:581-584.
75. Harry G.J., Lefebvre d'Hellencourt C. Dentate gyrus: alterations that occur with hippocampal injury. Neurotoxicology 2003, 24:343-356.
76. Havekes R., Vecsey C.G., Abel T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell Signal 2012, 24:1251-1260.
77. Heine J., Pruess H., Bartsch T., Ploner C.J., Paul F., Finke C. Imaging of autoimmune encephalitis - relevance for clinical practice and hippocampal function. Neuroscience 2015, 309:68-83.
78. Heneka M.T., Golenbock D.T., Latz E. Innate immunity in Alzheimer's disease. Nat Immunol 2015, 16:229-236.
79. Howland J.G., Wang Y.T. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 2008, 169:145-158.
80. Hughes E.G., Peng X., Gleichman A.J., Lai M., Zhou L., Tsou R., Parsons T.D., Lynch D.R., Dalmau J., Balice-Gordon R.J. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 2010, 30:5866-5875.
81. Hulme S.R., Jones O.D., Abraham W.C. Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci 2013, 36:353-362.
82. Hulst H.E., Schoonheim M.M., Roosendaal S.D., Popescu V., Schweren L.J., van der Werf Y.D., Visser L.H., Polman C.H., Barkhof F., Geurts J.J. Functional adaptive changes within the hippocampal memory system of patients with multiple sclerosis. Hum Brain Mapp 2012, 33:2268-2280.
83. Hunsaker M.R., Kesner R.P. The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neurosci Biobehav Rev 2013, 37:36-58.
84. Inagaki M., Yoshikawa E., Matsuoka Y., Sugawara Y., Nakano T., Akechi T., Wada N., Imoto S., Murakami K., Uchitomi Y. Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy. Cancer 2007, 109:146-156.
85. Irani S.R., Gelfand J.M., Al-Diwani A., Vincent A. Cell-surface central nervous system autoantibodies: clinical relevance and emerging paradigms. Ann Neurol 2014, 76:168-184.
86. Joels M. Stress, the hippocampus, and epilepsy. Epilepsia 2009, 50:586-597.
87. Jones O (2015) Astrocyte mediated metaplasticity in the hippocampus: Help or hindrance? Neuroscience 309:113-124.
88. Kaiser J., Bledowski C., Dietrich J. Neural correlates of chemotherapy-related cognitive impairment. Cortex 2014, 54:33-50.
89. Kayser M.S., Dalmau J. Anti-NMDA receptor encephalitis, autoimmunity, and psychosis. Schizophr Res 2014, 10.1016/j.schres.2014.10.007.
90. Kesner R.P., Hunsaker M.R. The temporal attributes of episodic memory. Behav Brain Res 2009, 215:299-309.
91. Kesner R.P., Rolls E.T. A computational theory of hippocampal function, and tests of the theory: new developments. Neurosci Biobehav Rev 2015, 48:92-147.
92. Kheirbek M.A., Klemenhagen K.C., Sahay A., Hen R. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 2012, 15:1613-1620.
93. Kienzler F., Norwood B.A., Sloviter R.S. Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J Comp Neurol 2009, 515:181-196.
94. Kirino T. Delayed neuronal death. Neuropathology 2000, 20(Suppl):S95-S97.
95. Kjelstrup K.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A 2002, 99:10825-10830.
96. Kolb B., Gibb R. Searching for the principles of brain plasticity and behavior. Cortex 2014, 58:251-260.
97. Kolb B., Muhammad A. Harnessing the power of neuroplasticity for intervention. Front Hum Neurosci 2014, 8:377.
98. Kostic M., Stojanovic I., Marjanovic G., Zivkovic N., Cvetanovic A. Deleterious versus protective autoimmunity in multiple sclerosis. Cell Immunol 2015, 296:122-132.
99. Kreutzmann J.C., Havekes R., Abel T., Meerlo P. Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience 2015, 309:173-190.
100. La Joie R., Fouquet M., Mezenge F., Landeau B., Villain N., Mevel K., Pelerin A., Eustache F., Desgranges B., Chetelat G. Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 2010, 53:506-514.
101. Lavenex P., Amaral D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 2000, 10:420-430.
102. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci 2010, 33:569-579.
103. Leuner B., Gould E. Structural plasticity and hippocampal function. Annu Rev Psychol 2010, 61(111-140):C111-C113.
104. Lisman J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 1999, 22:233-242.
105. Lisman J.E., Otmakhova N.A. Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 2001, 11:551-568.
106. Lister J.P., Barnes C.A. Neurobiological changes in the hippocampus during normative aging. Arch Neurol 2009, 66:829-833.
107. Lucassen P.J., Pruessner J., Sousa N., Almeida O.F., Van Dam A.M., Rajkowska G., Swaab D.F., Czeh B. Neuropathology of stress. Acta Neuropathol 2014, 127:109-135.
108. Malykhin N.V., Coupland N.J. Hippocampal neuroplasticity in major depressive disorder. Neuroscience 2015, 309:200-213.
109. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 1971, 262:23-81.
110. McEwen B. The plasticity of the hippocampus is the reason for its vulnerability. Semin Neurosci 1994, 6:239-246.
111. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007, 87:873-904.
112. McEwen B.S., Milner T.A. Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res Rev 2007, 55:343-355.
113. Michaelis E (2012) Selective Neuronal Vulnerability in the Hippocampus: Relationship to Neurological Diseases and Mechanisms for Differential Sensitivity of Neurons to Stress. In: The clinical neurobiology of the hippocampus (Th. Bartsch, ed), pp 54-76 Oxford: Oxford University Press.
114. Michailidou I., Willems J.G., Kooi E.J., van Eden C., Gold S.M., Geurts J.J., Baas F., Huitinga I., Ramaglia V. Complement C1q-C3 associated synaptic changes in multiple sclerosis hippocampus. Ann Neurol 2015, 77:1007-1026.
115. Michels M., Vieira A.S., Vuolo F., Zapelini H.G., Mendonca B., Mina F., Dominguini D., Steckert A., Schuck P.F., Quevedo J., Petronilho F., Dal-Pizzol F. The role of microglia activation in the development of sepsis-induced long-term cognitive impairment. Brain Behav Immun 2015, 43:54-59.
116. Miles D.K., Kernie S.G. Hypoxic-ischemic brain injury activates early hippocampal stem/progenitor cells to replace vulnerable neuroblasts. Hippocampus 2008, 18:793-806.
117. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
118. Monje M., Dietrich J. Cognitive side effects of cancer therapy demonstrate a functional role for adult neurogenesis. Behav Brain Res 2012, 227:376-379.
119. Moscato E.H., Jain A., Peng X., Hughes E.G., Dalmau J., Balice-Gordon R.J. Mechanisms underlying autoimmune synaptic encephalitis leading to disorders of memory, behavior and cognition: insights from molecular, cellular and synaptic studies. Eur J Neurosci 2010, 32:298-309.
120. Moser M.B., Moser E.I. Functional differentiation in the hippocampus. Hippocampus 1998, 8:608-619.
121. Mueller S.G., Chao L.L., Berman B., Weiner M.W. Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T. Neuroimage 2011, 56:851-857.
122. Mueller S.G., Schuff N., Yaffe K., Madison C., Miller B., Weiner M.W. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 2010, 31:1339-1347.
123. Mueller S.G., Stables L., Du A.T., Schuff N., Truran D., Cashdollar N., Weiner M.W. Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol Aging 2007, 28:719-726.
124. Mueller S.G., Weiner M.W. Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009, 19:558-564.
125. Mufson E.J., Mahady L., Waters D., Counts S.E., Perez S.E., DeKosky S.T., Ginsberg S.D., Ikonomovic M.D., Scheff S.W., Binder L.I. Hippocampal plasticity during the progression of Alzheimer's disease. Neuroscience 2015, 309:51-67.
126. Murray A.J., Sauer J.F., Riedel G., McClure C., Ansel L., Cheyne L., Bartos M., Wisden W., Wulff P. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nat Neurosci 2011, 14:297-299.
127. Neunuebel J.P., Knierim J.J. CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 2014, 81:416-427.
128. Newrzella D., Pahlavan P.S., Kruger C., Boehm C., Sorgenfrei O., Schrock H., Eisenhardt G., Bischoff N., Vogt G., Wafzig O., Rossner M., Maurer M.H., Hiemisch H., Bach A., Kuschinsky W., Schneider A. The functional genome of CA1 and CA3 neurons under native conditions and in response to ischemia. BMC Genomics 2007, 8:370.
129. Nistico R., Mori F., Feligioni M., Nicoletti F., Centonze D. Synaptic plasticity in multiple sclerosis and in experimental autoimmune encephalomyelitis. Philos Trans R Soc Lond B Biol Sci 2014, 369:20130162.
130. Novkovic T., Shchyglo O., Gold R., Manahan-Vaughan D. Hippocampal function is compromised in an animal model of multiple sclerosis. Neuroscience 2015, 309:100-112.
131. O'Dell C.M., Das A., Gt Wallace., Ray S.K., Banik N.L. Understanding the basic mechanisms underlying seizures in mesial temporal lobe epilepsy and possible therapeutic targets: a review. J Neurosci Res 2012, 90:913-924.
132. O'Neill J., Pleydell-Bouverie B., Dupret D., Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci 2010, 33:220-229.
133. O'Reilly R.C., McClelland J.L. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 1994, 4:661-682.
134. Olariu A., Cleaver K.M., Cameron H.A. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol 2007, 501:659-667.
135. Opendak M., Gould E. Adult neurogenesis: a substrate for experience-dependent change. Trends Cogn Sci 2015, 19:151-161.
136. Orban P., Rauchs G., Balteau E., Degueldre C., Luxen A., Maquet P., Peigneux P. Sleep after spatial learning promotes covert reorganization of brain activity. Proc Natl Acad Sci U S A 2006, 103:7124-7129.
137. Pandis C., Sotiriou E., Kouvaras E., Asprodini E., Papatheodoropoulos C., Angelatou F. Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus. Neuroscience 2006, 140:163-175.
138. Papadopoulos D., Dukes S., Patel R., Nicholas R., Vora A., Reynolds R. Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol 2009, 19:238-253.
139. Pastalkova E., Serrano P., Pinkhasova D., Wallace E., Fenton A.A., Sacktor T.C. Storage of spatial information by the maintenance mechanism of LTP. Science 2006, 313:1141-1144.
140. Peruga I., Hartwig S., Thone J., Hovemann B., Gold R., Juckel G., Linker R.A. Inflammation modulates anxiety in an animal model of multiple sclerosis. Behav Brain Res 2011, 220:20-29.
141. Pitkanen A., Sutula T.P. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 2002, 1:173-181.
142. Planagumà J., Leypoldt F., Mannara F., Gutiérrez-Cuesta J., Martín-García E., Aguilar E., Titulaer M., Jain A., Balice-Gordon R., Lakadamyali M., Graus F., Maldonado R., Dalmau J. Human N-Methyl-D-aspartate receptor antibodies alter memory and behavior in mice. Brain 2015, 138:94-109.
143. Poppenk J., Evensmoen H.R., Moscovitch M., Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn Sci 2013, 17:230-240.
144. Prince T.M., Abel T. The impact of sleep loss on hippocampal function. Learn Mem 2013, 20:558-569.
145. Pulsinelli W.A., Brierley J.B., Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 1982, 11:491-498.
146. Pun R.Y., Rolle I.J., Lasarge C.L., Hosford B.E., Rosen J.M., Uhl J.D., Schmeltzer S.N., Faulkner C., Bronson S.L., Murphy B.L., Richards D.A., Holland K.D., Danzer S.C. Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron 2012, 75:1022-1034.
147. Quintana P., Stefano A., Hakkoum D., Muller D. Glutamate receptor changes associated with transient anoxia/hypoglycaemia in hippocampal slice cultures. Eur J Neurosci 2006, 23:975-983.
148. Rolls E.T., Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 2006, 79:1-48.
149. Roosendaal S.D., Hulst H.E., Vrenken H., Feenstra H.E., Castelijns J.A., Pouwels P.J., Barkhof F., Geurts J.J. Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function. Radiology 2010, 255:595-604.
150. Roosendaal S.D., Moraal B., Vrenken H., Castelijns J.A., Pouwels P.J., Barkhof F., Geurts J.J. In vivo MR imaging of hippocampal lesions in multiple sclerosis. J Magn Reson Imaging 2008, 27:726-731.
151. Ryan T.J., Roy D.S., Pignatelli M., Arons A., Tonegawa S. Memory. Engram cells retain memory under retrograde amnesia. Science 2015, 348:1007-1013.
152. Sacco R., Bisecco A., Corbo D., Della Corte M., d'Ambrosio A., Docimo R., Gallo A., Esposito F., Esposito S., Cirillo M., Lavorgna L., Tedeschi G., Bonavita S. Cognitive impairment and memory disorders in relapsing-remitting multiple sclerosis: the role of white matter, gray matter and hippocampus. J Neurol 2015, 262:1691-1697.
153. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007, 10:1110-1115.
154. Sahay A., Wilson D.A., Hen R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 2011, 70:582-588.
155. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007, 2007:78970.
156. Schmidt-Kastner R., Freund T.F. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 1991, 40:599-636.
157. Schwamm L.H., Koroshetz W.J., Sorensen A.G., Wang B., Copen W.A., Budzik R., Rordorf G., Buonanno F.S., Schaefer P.W., Gonzalez R.G. Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging. Stroke 1998, 29:2268-2276.
158. Segal M., Richter-Levin G., Maggio N. Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 2010, 20:1332-1338.
159. Seigers R., Schagen S.B., Van Tellingen O., Dietrich J. Chemotherapy-related cognitive dysfunction: current animal studies and future directions. Brain Imaging Behav 2013, 7:453-459.
160. Semmler A., Widmann C.N., Okulla T., Urbach H., Kaiser M., Widman G., Mormann F., Weide J., Fliessbach K., Hoeft A., Jessen F., Putensen C., Heneka M.T. Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors. J Neurol Neurosurg Psychiatry 2013, 84:62-69.
161. Shing Y.L., Rodrigue K.M., Kennedy K.M., Fandakova Y., Bodammer N., Werkle-Bergner M., Lindenberger U., Raz N. Hippocampal subfield volumes: age, vascular risk, and correlation with associative memory. Front Aging Neurosci 2011, 3:2.
162. Sicotte N.L., Kern K.C., Giesser B.S., Arshanapalli A., Schultz A., Montag M., Wang H., Bookheimer S.Y. Regional hippocampal atrophy in multiple sclerosis. Brain 2008, 131:1134-1141.
163. Sierra A., Grohn O., Pitkanen A. Imaging microstructural damage and plasticity in the hippocampus during epileptogenesis. Neuroscience 2015, 309:162-172.
164. Sloviter R.S., Bumanglag A.V. Defining "epileptogenesis" and identifying "antiepileptogenic targets" in animal models of acquired temporal lobe epilepsy is not as simple as it might seem. Neuropharmacology 2013, 69:3-15.
165. Small S.A. The longitudinal axis of the hippocampal formation: its anatomy, circuitry, and role in cognitive function. Rev Neurosci 2002, 13:183-194.
166. Small S.A., Schobel S.A., Buxton R.B., Witter M.P., Barnes C.A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011, 12:585-601.
167. Stranahan A.M. Models and mechanisms for hippocampal dysfunction in obesity and diabetes. Neuroscience 2015, 309:125-139.
168. Stranahan A.M., Arumugam T.V., Cutler R.G., Lee K., Egan J.M., Mattson M.P. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 2008, 11:309-317.
169. Stranahan A.M., Mattson M.P. Bidirectional metabolic regulation of neurocognitive function. Neurobiol Learn Mem 2011, 96:507-516.
170. Strange B.A., Witter M.P., Lein E.S., Moser E.I. Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 2014, 15:655-669.
171. Suthana N.A., Ekstrom A.D., Moshirvaziri S., Knowlton B., Bookheimer S.Y. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J Neurosci 2009, 29:10512-10519.
172. Tamminga C.A., Suzanne Zukin R. Schizophrenia: evidence implicating hippocampal GluN2B protein and REST epigenetics in psychosis pathophysiology. Neuroscience 2015, 309:233-242.
173. Tan H., Cao J., Zhang J., Zuo Z. Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats. J Neuroinflammation 2014, 11:93.
174. Thompson C.L., Pathak S.D., Jeromin A., Ng L.L., MacPherson C.R., Mortrud M.T., Cusick A., Riley Z.L., Sunkin S.M., Bernard A., Puchalski R.B., Gage F.H., Jones A.R., Bajic V.B., Hawrylycz M.J., Lein E.S. Genomic anatomy of the hippocampus. Neuron 2008, 60:1010-1021.
175. Tononi G., Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 2014, 81:12-34.
176. Urbach H., Soeder B.M., Jeub M., Klockgether T., Meyer B., Bien C.G. Serial MRI of limbic encephalitis. Neuroradiology 2006, 48:380-386.
177. van der Marel K., Bouet V., Meerhoff G.F., Freret T., Boulouard M., Dauphin F., Klomp A., Lucassen P.J., Homberg J.R., Dijkhuizen R.M., Reneman L. Effects of long-term methylphenidate treatment in adolescent and adult rats on hippocampal shape, functional connectivity and adult neurogenesis. Neuroscience 2015, 309:243-258.
178. van Strien N.M., Cappaert N.L., Witter M.P. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 2009, 10:272-282.
179. Varley J., Vincent A., Irani S.R. Clinical and experimental studies of potentially pathogenic brain-directed autoantibodies: current knowledge and future directions. J Neurol 2015, 262:1081-1095.
180. Voss M.W., Vivar C., Kramer A.F., van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci 2013, 17:525-544.
181. Wang X., Michaelis E.K. Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2010, 2:12.
182. Wegner C., Stadelmann C. Gray matter pathology and multiple sclerosis. Curr Neurol Neurosci Rep 2009, 9:399-404.
183. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772.
184. Williamson L.L., Bilbo S.D. Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability. Brain Behav Immun 2013, 30:186-194.
185. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
186. Wisse L.E., Biessels G.J., Heringa S.M., Kuijf H.J., Koek D.H., Luijten P.R., Geerlings M.I. Hippocampal subfield volumes at 7T in early Alzheimer's disease and normal aging. Neurobiol Aging 2014, 35:2039-2045.
187. Wu M.V., Hen R. Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus 2014, 24:751-761.
188. Wulff P., Ponomarenko A.A., Bartos M., Korotkova T.M., Fuchs E.C., Bahner F., Both M., Tort A.B., Kopell N.J., Wisden W., Monyer H. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 2009, 106:3561-3566.
189. Yang Y., Song W. Molecular links between Alzheimer's disease and diabetes mellitus. Neuroscience 2013, 250:140-150.
190. Yassa M.A., Mattfeld A.T., Stark S.M., Stark C.E. Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proc Natl Acad Sci U S A 2011, 108:8873-8878.
191. Yassa M.A., Stark C.E. Pattern separation in the hippocampus. Trends Neurosci 2011, 34:515-525.