The hippocampus in aging and disease: From plasticity to vulnerability

Neuroscience - Tập 309 - Trang 1-16 - 2015
T. Bartsch1, P. Wulff2
1Department of Neurology, Memory Disorders and Plasticity Group, University Hospital Schleswig-Holstein, Kiel, Germany
2Institute of Physiology, Neurophysiology, University of Kiel, Olshausenstrasse 40, 24098 Kiel, Germany

Tài liệu tham khảo

Aimone, 2014, Regulation and function of adult neurogenesis: from genes to cognition, Physiol Rev, 94, 991, 10.1152/physrev.00004.2014 Aksoy-Aksel, 2015, 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, 309, 191, 10.1016/j.neuroscience.2015.03.014 Amaral, 2007, The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies), Prog Brain Res, 163, 3, 10.1016/S0079-6123(07)63001-5 Anderson, 2010, Hippocampal atrophy in relapsing-remitting and primary progressive MS: a comparative study, Mult Scler, 16, 1083, 10.1177/1352458510374893 Avignone, 2005, Differential responses to NMDA receptor activation in rat hippocampal interneurons and pyramidal cells may underlie enhanced pyramidal cell vulnerability, Eur J Neurosci, 22, 3077, 10.1111/j.1460-9568.2005.04497.x Baier, 2009, Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice, Behav Brain Res, 200, 192, 10.1016/j.bbr.2009.01.013 Bakker, 2008, Pattern separation in the human hippocampal CA3 and dentate gyrus, Science, 319, 1640, 10.1126/science.1152882 Bannerman, 2004, Regional dissociations within the hippocampus–memory and anxiety, Neurosci Biobehav Rev, 28, 273, 10.1016/j.neubiorev.2004.03.004 Barrientos, 2012, Aging-related changes in neuroimmune-endocrine function: implications for hippocampal-dependent cognition, Horm Behav, 62, 219, 10.1016/j.yhbeh.2012.02.010 Barrientos, 2015, Neuroinflammation in the normal aging hippocampus, Neuroscience, 309, 84, 10.1016/j.neuroscience.2015.03.007 Bartsch, 2012 Bartsch, 2006, Selective affection of hippocampal CA-1 neurons in patients with transient global amnesia without long-term sequelae, Brain, 129, 2874, 10.1093/brain/awl248 Bartsch, 2008, Focal MR spectroscopy of hippocampal CA-1 lesions in transient global amnesia, Neurology, 70, 1030, 10.1212/01.wnl.0000306633.06027.33 Bartsch, 2011, CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness, Proc Natl Acad Sci U S A, 108, 17562, 10.1073/pnas.1110266108 Bartsch, 2015, 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, 10.1038/jcbfm.2015.137 Bartsch, 2010, Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory, Science, 328, 1412, 10.1126/science.1188160 Battaglia, 2011, The hippocampus: hub of brain network communication for memory, Trends Cognit Sci, 15, 310 Bendel, 2005, Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory, J Cereb Blood Flow Metab, 25, 1586, 10.1038/sj.jcbfm.9600153 Bergmann, 2013, Neuroscience. Why adults need new brain cells, Science, 340, 695, 10.1126/science.1237976 Bettcher, 2014, More than memory impairment in voltage-gated potassium channel complex encephalopathy, Eur J Neurol, 21, 1301, 10.1111/ene.12482 Bien, 2007, Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy, Neurology, 69, 1236, 10.1212/01.wnl.0000276946.08412.ef Bliss, 2004, Neuroscience. Controlling the ups and downs of synaptic strength, Science, 304, 973, 10.1126/science.1098805 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. Bonnici, 2012, Multi-voxel pattern analysis in human hippocampal subfields, Front Hum Neurosci, 6, 290, 10.3389/fnhum.2012.00290 Bonnici, 2013, Representations of recent and remote autobiographical memories in hippocampal subfields, Hippocampus, 23, 849, 10.1002/hipo.22155 Braak, 1995, Staging of Alzheimer’s disease-related neurofibrillary changes, Neurobiol Aging, 16, 271, 10.1016/0197-4580(95)00021-6 Braak, 1996, Evolution of the neuropathology of Alzheimer’s disease, Acta Neurol Scand Suppl, 165, 3, 10.1111/j.1600-0404.1996.tb05866.x Brainin, 1988, Structural brain correlates of anterograde memory deficits in multiple sclerosis, J Neurol, 235, 362, 10.1007/BF00314234 Braun, 2013, Effects of blockade of peripheral interleukin-6 trans-signaling on hippocampus-dependent and independent memory in mice, J Interferon Cytokine Res, 33, 254, 10.1089/jir.2012.0096 Brown, 2003, Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis, Eur J Neurosci, 17, 2042, 10.1046/j.1460-9568.2003.02647.x Bueters, 2008, Degeneration of newly formed CA1 neurons following global ischemia in the rat, Exp Neurol, 209, 114, 10.1016/j.expneurol.2007.09.005 Burger, 2010, Region-specific genetic alterations in the aging hippocampus: implications for cognitive aging, Front Aging Neurosci, 2, 140, 10.3389/fnagi.2010.00140 Burke, 2006, Neural plasticity in the ageing brain, Nat Rev Neurosci, 7, 30, 10.1038/nrn1809 Burke, 2010, Senescent synapses and hippocampal circuit dynamics, Trends Neurosci, 33, 153, 10.1016/j.tins.2009.12.003 Butler, 2010, 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, 165, 525, 10.1016/j.neuroscience.2009.10.018 Buzsaki, 2013, Memory, navigation and theta rhythm in the hippocampal-entorhinal system, Nat Neurosci, 16, 130, 10.1038/nn.3304 Carpentier, 2009, Immune influence on adult neural stem cell regulation and function, Neuron, 64, 79, 10.1016/j.neuron.2009.08.038 Cendes, 2014, Epilepsies associated with hippocampal sclerosis, Acta Neuropathol, 128, 21, 10.1007/s00401-014-1292-0 Chen, 2009, Behavioral deficits and subregion-specific suppression of LTP in mice expressing a population of mutant NMDA receptors throughout the hippocampus, Learn Mem, 16, 635, 10.1101/lm.1316909 Chetelat, 2008, Three-dimensional surface mapping of hippocampal atrophy progression from MCI to AD and over normal aging as assessed using voxel-based morphometry, Neuropsychologia, 46, 1721, 10.1016/j.neuropsychologia.2007.11.037 Coultrap, 2005, 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, 135, 104, 10.1016/j.molbrainres.2004.12.005 Cramer, 2011, Harnessing neuroplasticity for clinical applications, Brain, 134, 1591, 10.1093/brain/awr039 Czepiel, 2015, Human oligodendrocytes in remyelination research, Glia, 63, 513, 10.1002/glia.22769 Das, 2012, Measuring longitudinal change in the hippocampal formation from in vivo high-resolution T2-weighted MRI, Neuroimage, 60, 1266, 10.1016/j.neuroimage.2012.01.098 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. de Flores, 2015, Effects of age and Alzheimer’s disease on hippocampal subfields: comparison between manual and FreeSurfer volumetry, Hum Brain Mapp, 36, 463, 10.1002/hbm.22640 de Kloet, 2005, Stress and the brain: from adaptation to disease, Nat Rev Neurosci, 6, 463, 10.1038/nrn1683 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. Deng, 2010, New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?, Nat Rev Neurosci, 11, 339, 10.1038/nrn2822 Deuker, 2014, Human neuroimaging studies on the hippocampal CA3 region – integrating evidence for pattern separation and completion, Front Cell Neurosci, 8, 64, 10.3389/fncel.2014.00064 Diekelmann, 2010, The memory function of sleep, Nat Rev Neurosci, 11, 114, 10.1038/nrn2762 Dietrich, 2015, Chemotherapy, cognitive impairment and hippocampal toxicity, Neuroscience, 309, 224, 10.1016/j.neuroscience.2015.06.016 Dohring, 2014, Stress-related factors in the emergence of transient global amnesia with hippocampal lesions, Front Behav Neurosci, 8, 287 Dong, 2009, Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1, Proc Natl Acad Sci U S A, 106, 11794, 10.1073/pnas.0812608106 Drapeau, 2003, Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis, Proc Natl Acad Sci U S A, 100, 14385, 10.1073/pnas.2334169100 Dutta, 2011, Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients, Ann Neurol, 69, 445, 10.1002/ana.22337 Dutta, 2013, Hippocampal demyelination and memory dysfunction are associated with increased levels of the neuronal microRNA miR-124 and reduced AMPA receptors, Ann Neurol, 73, 637, 10.1002/ana.23860 Engvig, 2012, Hippocampal subfield volumes correlate with memory training benefit in subjective memory impairment, Neuroimage, 61, 188, 10.1016/j.neuroimage.2012.02.072 Erion, 2014, Obesity elicits interleukin 1-mediated deficits in hippocampal synaptic plasticity, J Neurosci, 34, 2618, 10.1523/JNEUROSCI.4200-13.2014 Falkai P, Gruber O, Schmitt A (2012) Schizophrenia. In: The clinical neurobiology of the hippocampus (Th. Bartsch, ed). Oxford: Oxford University Press. Fanselow, 2010, Are the dorsal and ventral hippocampus functionally distinct structures?, Neuron, 65, 7, 10.1016/j.neuron.2009.11.031 Finke, 2013, Neural correlates of short-term memory reorganization in humans with hippocampal damage, J Neurosci, 33, 11061, 10.1523/JNEUROSCI.0744-13.2013 Finke, 2013, Functional and structural brain changes in anti-N-methyl-D-aspartate receptor encephalitis, Ann Neurol, 74, 284 Fontan-Lozano, 2007, Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor, J Neurosci, 27, 10185, 10.1523/JNEUROSCI.2757-07.2007 Forster, 2012, Diffusion-weighted imaging for the differential diagnosis of disorders affecting the hippocampus, Cerebrovasc Dis, 33, 104, 10.1159/000332036 Fotuhi, 2012, Modifiable factors that alter the size of the hippocampus with ageing, Nat Rev Neurol, 8, 189, 10.1038/nrneurol.2012.27 Fouquet, 2012, Role of hippocampal CA1 atrophy in memory encoding deficits in amnestic mild cognitive impairment, Neuroimage, 59, 3309, 10.1016/j.neuroimage.2011.11.036 Freund, 2013, Emergence of individuality in genetically identical mice, Science, 340, 756, 10.1126/science.1235294 Gee, 2006, NMDA receptors and the differential ischemic vulnerability of hippocampal neurons, Eur J Neurosci, 23, 2595, 10.1111/j.1460-9568.2006.04786.x Geurts, 2007, Extensive hippocampal demyelination in multiple sclerosis, J Neuropathol Exp Neurol, 66, 819, 10.1097/nen.0b013e3181461f54 Gold, 2010, Smaller cornu ammonis 2–3/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms, Biol Psychiatry, 68, 553, 10.1016/j.biopsych.2010.04.025 Gold, 2014, Detection of altered hippocampal morphology in multiple sclerosis-associated depression using automated surface mesh modeling, Hum Brain Mapp, 35, 30, 10.1002/hbm.22154 Gray DT, Barnes CA (2015) Distinguishing adaptive plasticity from vulnerability in the aging hippocampus. Neuroscience 309:17–28. Guzowski, 2004, Ensemble dynamics of hippocampal regions CA3 and CA1, Neuron, 44, 581, 10.1016/j.neuron.2004.11.003 Harry, 2003, Dentate gyrus: alterations that occur with hippocampal injury, Neurotoxicology, 24, 343, 10.1016/S0161-813X(03)00039-1 Havekes, 2012, The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity, Cell Signal, 24, 1251, 10.1016/j.cellsig.2012.02.010 Heine, 2015, Imaging of autoimmune encephalitis – relevance for clinical practice and hippocampal function, Neuroscience, 309, 68, 10.1016/j.neuroscience.2015.05.037 Heneka, 2015, Innate immunity in Alzheimer’s disease, Nat Immunol, 16, 229, 10.1038/ni.3102 Howland, 2008, Synaptic plasticity in learning and memory: stress effects in the hippocampus, Prog Brain Res, 169, 145, 10.1016/S0079-6123(07)00008-8 Hughes, 2010, Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis, J Neurosci, 30, 5866, 10.1523/JNEUROSCI.0167-10.2010 Hulme, 2013, Emerging roles of metaplasticity in behaviour and disease, Trends Neurosci, 36, 353, 10.1016/j.tins.2013.03.007 Hulst, 2012, Functional adaptive changes within the hippocampal memory system of patients with multiple sclerosis, Hum Brain Mapp, 33, 2268, 10.1002/hbm.21359 Hunsaker, 2013, The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory, Neurosci Biobehav Rev, 37, 36, 10.1016/j.neubiorev.2012.09.014 Inagaki, 2007, Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy, Cancer, 109, 146, 10.1002/cncr.22368 Irani, 2014, Cell-surface central nervous system autoantibodies: clinical relevance and emerging paradigms, Ann Neurol, 76, 168, 10.1002/ana.24200 Joels, 2009, Stress, the hippocampus, and epilepsy, Epilepsia, 50, 586, 10.1111/j.1528-1167.2008.01902.x Jones O (2015) Astrocyte mediated metaplasticity in the hippocampus: Help or hindrance? Neuroscience 309:113–124. Kaiser, 2014, Neural correlates of chemotherapy-related cognitive impairment, Cortex, 54, 33, 10.1016/j.cortex.2014.01.010 Kayser, 2014, Anti-NMDA receptor encephalitis, autoimmunity, and psychosis, Schizophr Res, 10.1016/j.schres.2014.10.007 Kesner, 2009, The temporal attributes of episodic memory, Behav Brain Res, 215, 299, 10.1016/j.bbr.2009.12.029 Kesner, 2015, A computational theory of hippocampal function, and tests of the theory: new developments, Neurosci Biobehav Rev, 48, 92, 10.1016/j.neubiorev.2014.11.009 Kheirbek, 2012, Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders, Nat Neurosci, 15, 1613, 10.1038/nn.3262 Kienzler, 2009, Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse, J Comp Neurol, 515, 181, 10.1002/cne.22059 Kirino, 2000, Delayed neuronal death, Neuropathology, 20, S95, 10.1046/j.1440-1789.2000.00306.x Kjelstrup, 2002, Reduced fear expression after lesions of the ventral hippocampus, Proc Natl Acad Sci U S A, 99, 10825, 10.1073/pnas.152112399 Kolb, 2014, Searching for the principles of brain plasticity and behavior, Cortex, 58, 251, 10.1016/j.cortex.2013.11.012 Kolb, 2014, Harnessing the power of neuroplasticity for intervention, Front Hum Neurosci, 8, 377, 10.3389/fnhum.2014.00377 Kostic, 2015, Deleterious versus protective autoimmunity in multiple sclerosis, Cell Immunol, 296, 122, 10.1016/j.cellimm.2015.04.006 Kreutzmann, 2015, Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function, Neuroscience, 309, 173, 10.1016/j.neuroscience.2015.04.053 La Joie, 2010, Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence, Neuroimage, 53, 506, 10.1016/j.neuroimage.2010.06.024 Lavenex, 2000, Hippocampal-neocortical interaction: a hierarchy of associativity, Hippocampus, 10, 420, 10.1002/1098-1063(2000)10:4<420::AID-HIPO8>3.0.CO;2-5 Lazarov, 2010, When neurogenesis encounters aging and disease, Trends Neurosci, 33, 569, 10.1016/j.tins.2010.09.003 Leuner, 2010, Structural plasticity and hippocampal function, Annu Rev Psychol, 61, C111, 10.1146/annurev.psych.093008.100359 Lisman, 1999, Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions, Neuron, 22, 233, 10.1016/S0896-6273(00)81085-5 Lisman, 2001, 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, 11, 551, 10.1002/hipo.1071 Lister, 2009, Neurobiological changes in the hippocampus during normative aging, Arch Neurol, 66, 829, 10.1001/archneurol.2009.125 Lucassen, 2014, Neuropathology of stress, Acta Neuropathol, 127, 109, 10.1007/s00401-013-1223-5 Malykhin, 2015, Hippocampal neuroplasticity in major depressive disorder, Neuroscience, 309, 200, 10.1016/j.neuroscience.2015.04.047 Marr, 1971, Simple memory: a theory for archicortex, Philos Trans R Soc Lond B Biol Sci, 262, 23, 10.1098/rstb.1971.0078 McEwen, 1994, The plasticity of the hippocampus is the reason for its vulnerability, Semin Neurosci, 6, 239, 10.1006/smns.1994.1031 McEwen, 2007, Physiology and neurobiology of stress and adaptation: central role of the brain, Physiol Rev, 87, 873, 10.1152/physrev.00041.2006 McEwen, 2007, Hippocampal formation: shedding light on the influence of sex and stress on the brain, Brain Res Rev, 55, 343, 10.1016/j.brainresrev.2007.02.006 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. Michailidou, 2015, Complement C1q-C3 associated synaptic changes in multiple sclerosis hippocampus, Ann Neurol, 77, 1007, 10.1002/ana.24398 Michels, 2015, The role of microglia activation in the development of sepsis-induced long-term cognitive impairment, Brain Behav Immun, 43, 54, 10.1016/j.bbi.2014.07.002 Miles, 2008, Hypoxic-ischemic brain injury activates early hippocampal stem/progenitor cells to replace vulnerable neuroblasts, Hippocampus, 18, 793, 10.1002/hipo.20439 Ming, 2011, Adult neurogenesis in the mammalian brain: significant answers and significant questions, Neuron, 70, 687, 10.1016/j.neuron.2011.05.001 Monje, 2012, Cognitive side effects of cancer therapy demonstrate a functional role for adult neurogenesis, Behav Brain Res, 227, 376, 10.1016/j.bbr.2011.05.012 Moscato, 2010, Mechanisms underlying autoimmune synaptic encephalitis leading to disorders of memory, behavior and cognition: insights from molecular, cellular and synaptic studies, Eur J Neurosci, 32, 298, 10.1111/j.1460-9568.2010.07349.x Moser, 1998, Functional differentiation in the hippocampus, Hippocampus, 8, 608, 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7 Mueller, 2011, Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T, Neuroimage, 56, 851, 10.1016/j.neuroimage.2011.03.028 Mueller, 2010, Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease, Hum Brain Mapp, 31, 1339, 10.1002/hbm.20934 Mueller, 2007, Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T, Neurobiol Aging, 28, 719, 10.1016/j.neurobiolaging.2006.03.007 Mueller, 2009, Selective effect of age, Apo e4, and Alzheimer’s disease on hippocampal subfields, Hippocampus, 19, 558, 10.1002/hipo.20614 Mufson, 2015, Hippocampal plasticity during the progression of Alzheimer’s disease, Neuroscience, 309, 51, 10.1016/j.neuroscience.2015.03.006 Murray, 2011, Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory, Nat Neurosci, 14, 297, 10.1038/nn.2751 Neunuebel, 2014, CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation, Neuron, 81, 416, 10.1016/j.neuron.2013.11.017 Newrzella, 2007, The functional genome of CA1 and CA3 neurons under native conditions and in response to ischemia, BMC Genomics, 8, 370, 10.1186/1471-2164-8-370 Nistico, 2014, Synaptic plasticity in multiple sclerosis and in experimental autoimmune encephalomyelitis, Philos Trans R Soc Lond B Biol Sci, 369, 20130162, 10.1098/rstb.2013.0162 Novkovic, 2015, Hippocampal function is compromised in an animal model of multiple sclerosis, Neuroscience, 309, 100, 10.1016/j.neuroscience.2015.03.008 O’Dell, 2012, Understanding the basic mechanisms underlying seizures in mesial temporal lobe epilepsy and possible therapeutic targets: a review, J Neurosci Res, 90, 913, 10.1002/jnr.22829 O’Neill, 2010, Play it again: reactivation of waking experience and memory, Trends Neurosci, 33, 220, 10.1016/j.tins.2010.01.006 O’Reilly, 1994, Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off, Hippocampus, 4, 661, 10.1002/hipo.450040605 Olariu, 2007, Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle, J Comp Neurol, 501, 659, 10.1002/cne.21268 Opendak, 2015, Adult neurogenesis: a substrate for experience-dependent change, Trends Cogn Sci, 19, 151, 10.1016/j.tics.2015.01.001 Orban, 2006, Sleep after spatial learning promotes covert reorganization of brain activity, Proc Natl Acad Sci U S A, 103, 7124, 10.1073/pnas.0510198103 Pandis, 2006, Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus, Neuroscience, 140, 163, 10.1016/j.neuroscience.2006.02.003 Papadopoulos, 2009, Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis, Brain Pathol, 19, 238, 10.1111/j.1750-3639.2008.00177.x Pastalkova, 2006, Storage of spatial information by the maintenance mechanism of LTP, Science, 313, 1141, 10.1126/science.1128657 Peruga, 2011, Inflammation modulates anxiety in an animal model of multiple sclerosis, Behav Brain Res, 220, 20, 10.1016/j.bbr.2011.01.018 Pitkanen, 2002, Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy, Lancet Neurol, 1, 173, 10.1016/S1474-4422(02)00073-X Planagumà, 2015, Human N-Methyl-D-aspartate receptor antibodies alter memory and behavior in mice, Brain, 138, 94, 10.1093/brain/awu310 Poppenk, 2013, Long-axis specialization of the human hippocampus, Trends Cogn Sci, 17, 230, 10.1016/j.tics.2013.03.005 Prince, 2013, The impact of sleep loss on hippocampal function, Learn Mem, 20, 558, 10.1101/lm.031674.113 Pulsinelli, 1982, Temporal profile of neuronal damage in a model of transient forebrain ischemia, Ann Neurol, 11, 491, 10.1002/ana.410110509 Pun, 2012, Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy, Neuron, 75, 1022, 10.1016/j.neuron.2012.08.002 Quintana, 2006, Glutamate receptor changes associated with transient anoxia/hypoglycaemia in hippocampal slice cultures, Eur J Neurosci, 23, 975, 10.1111/j.1460-9568.2006.04617.x Rolls, 2006, A computational theory of hippocampal function, and empirical tests of the theory, Prog Neurobiol, 79, 1, 10.1016/j.pneurobio.2006.04.005 Roosendaal, 2010, Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function, Radiology, 255, 595, 10.1148/radiol.10091433 Roosendaal, 2008, In vivo MR imaging of hippocampal lesions in multiple sclerosis, J Magn Reson Imaging, 27, 726, 10.1002/jmri.21294 Ryan, 2015, Memory. Engram cells retain memory under retrograde amnesia, Science, 348, 1007, 10.1126/science.aaa5542 Sacco, 2015, Cognitive impairment and memory disorders in relapsing-remitting multiple sclerosis: the role of white matter, gray matter and hippocampus, J Neurol, 262, 1691, 10.1007/s00415-015-7763-y Sahay, 2007, Adult hippocampal neurogenesis in depression, Nat Neurosci, 10, 1110, 10.1038/nn1969 Sahay, 2011, Pattern separation: a common function for new neurons in hippocampus and olfactory bulb, Neuron, 70, 582, 10.1016/j.neuron.2011.05.012 Sandi, 2007, Stress and memory: behavioral effects and neurobiological mechanisms, Neural Plast, 2007, 78970, 10.1155/2007/78970 Schmidt-Kastner, 1991, Selective vulnerability of the hippocampus in brain ischemia, Neuroscience, 40, 599, 10.1016/0306-4522(91)90001-5 Schwamm, 1998, Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging, Stroke, 29, 2268, 10.1161/01.STR.29.11.2268 Segal, 2010, Stress-induced dynamic routing of hippocampal connectivity: a hypothesis, Hippocampus, 20, 1332, 10.1002/hipo.20751 Seigers, 2013, Chemotherapy-related cognitive dysfunction: current animal studies and future directions, Brain Imaging Behav, 7, 453, 10.1007/s11682-013-9250-3 Semmler, 2013, Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors, J Neurol Neurosurg Psychiatry, 84, 62, 10.1136/jnnp-2012-302883 Shing, 2011, Hippocampal subfield volumes: age, vascular risk, and correlation with associative memory, Front Aging Neurosci, 3, 2, 10.3389/fnagi.2011.00002 Sicotte, 2008, Regional hippocampal atrophy in multiple sclerosis, Brain, 131, 1134, 10.1093/brain/awn030 Sierra, 2015, Imaging microstructural damage and plasticity in the hippocampus during epileptogenesis, Neuroscience, 309, 162, 10.1016/j.neuroscience.2015.04.054 Sloviter, 2013, Defining “epileptogenesis” and identifying “antiepileptogenic targets” in animal models of acquired temporal lobe epilepsy is not as simple as it might seem, Neuropharmacology, 69, 3, 10.1016/j.neuropharm.2012.01.022 Small, 2002, The longitudinal axis of the hippocampal formation: its anatomy, circuitry, and role in cognitive function, Rev Neurosci, 13, 183, 10.1515/REVNEURO.2002.13.2.183 Small, 2011, A pathophysiological framework of hippocampal dysfunction in ageing and disease, Nat Rev Neurosci, 12, 585, 10.1038/nrn3085 Stranahan, 2015, Models and mechanisms for hippocampal dysfunction in obesity and diabetes, Neuroscience, 309, 125, 10.1016/j.neuroscience.2015.04.045 Stranahan, 2008, Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons, Nat Neurosci, 11, 309, 10.1038/nn2055 Stranahan, 2011, Bidirectional metabolic regulation of neurocognitive function, Neurobiol Learn Mem, 96, 507, 10.1016/j.nlm.2011.01.004 Strange, 2014, Functional organization of the hippocampal longitudinal axis, Nat Rev Neurosci, 15, 655, 10.1038/nrn3785 Suthana, 2009, Human hippocampal CA1 involvement during allocentric encoding of spatial information, J Neurosci, 29, 10512, 10.1523/JNEUROSCI.0621-09.2009 Tamminga, 2015, Schizophrenia: evidence implicating hippocampal GluN2B protein and REST epigenetics in psychosis pathophysiology, Neuroscience, 309, 233, 10.1016/j.neuroscience.2015.07.038 Tan, 2014, Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats, J Neuroinflammation, 11, 93, 10.1186/1742-2094-11-93 Thompson, 2008, Genomic anatomy of the hippocampus, Neuron, 60, 1010, 10.1016/j.neuron.2008.12.008 Tononi, 2014, Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration, Neuron, 81, 12, 10.1016/j.neuron.2013.12.025 Urbach, 2006, Serial MRI of limbic encephalitis, Neuroradiology, 48, 380, 10.1007/s00234-006-0069-0 van der Marel, 2015, Effects of long-term methylphenidate treatment in adolescent and adult rats on hippocampal shape, functional connectivity and adult neurogenesis, Neuroscience, 309, 243, 10.1016/j.neuroscience.2015.04.044 van Strien, 2009, The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network, Nat Rev Neurosci, 10, 272, 10.1038/nrn2614 Varley, 2015, Clinical and experimental studies of potentially pathogenic brain-directed autoantibodies: current knowledge and future directions, J Neurol, 262, 1081, 10.1007/s00415-014-7600-8 Voss, 2013, Bridging animal and human models of exercise-induced brain plasticity, Trends Cogn Sci, 17, 525, 10.1016/j.tics.2013.08.001 Wang, 2010, Selective neuronal vulnerability to oxidative stress in the brain, Front Aging Neurosci, 2, 12 Wegner, 2009, Gray matter pathology and multiple sclerosis, Curr Neurol Neurosci Rep, 9, 399, 10.1007/s11910-009-0058-x West, 1994, Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer’s disease, Lancet, 344, 769, 10.1016/S0140-6736(94)92338-8 Williamson, 2013, Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability, Brain Behav Immun, 30, 186, 10.1016/j.bbi.2013.01.077 Wilson, 1994, Reactivation of hippocampal ensemble memories during sleep, Science, 265, 676, 10.1126/science.8036517 Wisse, 2014, Hippocampal subfield volumes at 7T in early Alzheimer’s disease and normal aging, Neurobiol Aging, 35, 2039, 10.1016/j.neurobiolaging.2014.02.021 Wu, 2014, Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus, Hippocampus, 24, 751, 10.1002/hipo.22265 Wulff, 2009, Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons, Proc Natl Acad Sci U S A, 106, 3561, 10.1073/pnas.0813176106 Yang, 2013, Molecular links between Alzheimer’s disease and diabetes mellitus, Neuroscience, 250, 140, 10.1016/j.neuroscience.2013.07.009 Yassa, 2011, Age-related memory deficits linked to circuit-specific disruptions in the hippocampus, Proc Natl Acad Sci U S A, 108, 8873, 10.1073/pnas.1101567108 Yassa, 2011, Pattern separation in the hippocampus, Trends Neurosci, 34, 515, 10.1016/j.tins.2011.06.006