Selective neuronal vulnerability of human hippocampal CA1 neurons: Lesion evolution, temporal course, and pattern of hippocampal damage in diffusion-weighted MR imaging

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 11, 2015, Pages 1836-1845

  Bartsch, Thorsten ^a   Döhring, Juliane ^a   Reuter, Sigrid ^a   Finke, Carsten ^b   Rohr, Axel ^a   Brauer, Henriette ^a   Deuschl, Günther ^a   Jansen, Olav ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

CA1; encephalitis; hippocampus; memory; stroke; vulnerability

Indexed keywords

ADULT; AMNESIA; AMYGDALOID NUCLEUS; APHASIA; APPARENT DIFFUSION COEFFICIENT; ARTICLE; BRAIN ARTERY; BRAIN ISCHEMIA; BRAIN STEM; CELL METABOLISM; CEREBROSPINAL FLUID; CINGULATE GYRUS; COMA; DELIRIUM; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; EPILEPTIC STATE; FEMALE; HERPES SIMPLEX ENCEPHALITIS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL ISCHEMIA; HIPPOCAMPUS; HUMAN; HYPERTENSION; HYPOTHALAMUS; INSULA; MAJOR CLINICAL STUDY; MALE; MEDIAL TEMPORAL LOBE; MIGRAINE; NERVE CELL; NERVOUS SYSTEM PARAMETERS; PARANEOPLASTIC NEUROPATHY; POSTERIOR CEREBRAL ARTERY; POSTERIOR INFERIOR CEREBELLAR ARTERY; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; RETROSPECTIVE STUDY; SELECTIVE NEURONAL VULNERABILITY; SUPERIOR CEREBELLAR ARTERY; TRANSIENT GLOBAL AMNESIA; VERTEBROBASILAR TERRITORY; AGED; BRAIN HYPOXIA; CEREBROVASCULAR DISEASE; CLASSIFICATION; COHORT ANALYSIS; ENCEPHALITIS; IMAGE PROCESSING; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; RISK FACTOR;

ADULT; AGED; AMNESIA, TRANSIENT GLOBAL; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; CEREBROVASCULAR DISORDERS; COHORT STUDIES; DIFFUSION MAGNETIC RESONANCE IMAGING; ENCEPHALITIS; FEMALE; HIPPOCAMPUS; HUMANS; HYPOXIA, BRAIN; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MIDDLE AGED; NEURONS; RISK FACTORS; STATUS EPILEPTICUS;

EID: 84946497436     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.137     Document Type: Article

References (41)

1. Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 1991; 40: 599-636.
2. Kirino T. Delayed neuronal death. Neuropathology 2000; 20: S95-S97.
3. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 1982; 239: 57-69.
4. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 1982; 11: 491-498.
5. Wang X, Michaelis EK. Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2010; 2: 12.
6. Bartsch T, Schonfeld R, Muller FJ, Alfke K, Leplow B, Aldenhoff J, et al. Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory. Science 2010; 328: 1412-1415.
7. Kadar T, Dachir S, Shukitt-Hale B, Levy A. Sub-regional hippocampal vulnerability in various animal models leading to cognitive dysfunction. J Neural Transm 1998; 105: 987-1004.
8. Forster A, Griebe M, Gass A, Kern R, Hennerici MG, Szabo K. Diffusion-weighted imaging for the differential diagnosis of disorders affecting the hippocampus. Cerebrovasc Dis 2012; 33: 104-115.
9. Szabo K, Forster A, Gass A. Conventional and diffusion-weighted MRI of the hippocampus. Front Neurol Neurosci 2014; 34: 71-84.
10. Anderova M, Vorisek I, Pivonkova H, Benesova J, Vargova L, Cicanic M, et al. Cell death/proliferation and alterations in glial morphology contribute to changes in diffusivity in the rat hippocampus after hypoxia-ischemia. J Cereb Blood Flow Metab 2010; 31: 894-907.
11. Szabo K, Forster A, Jager T, Kern R, Griebe M, Hennerici MG, et al. Hippocampal lesion patterns in acute posterior cerebral artery stroke: clinical and MRI findings. Stroke 2009; 40: 2042-2045.
12. Hatipoglu HG, Sakman B, Yuksel E. Magnetic resonance and diffusion-weighted imaging findings of herpes simplex encephalitis. Herpes 2008; 15: 13-17.
13. Urbach H, Soeder BM, Jeub M, Klockgether T, Meyer B, Bien CG. Serial MRI of limbic encephalitis. Neuroradiology 2006; 48: 380-386.
14. Parmar H, Lim SH, Tan NC, Lim CC. Acute symptomatic seizures and hippocampus damage: DWI and MRS findings. Neurology 2006; 66: 1732-1735.
15. Bartsch T, Alfke K, Deuschl G, Jansen O. Evolution of hippocampal CA-1 diffusion lesions in transient global amnesia. Ann Neurol 2007; 62: 475-480.
16. Bartsch T, Döhring J, Brauer H, Lagies J, Rohr A, Deuschl G, et al. Selective neuronal vulnerability of hippocampal CA1 neurons in acute neurological disorders. Neuroscience 2013. Society for Neuroscience: San Diego, USA, 2013.
17. Enzinger C, Thimary F, Kapeller P, Ropele S, Schmidt R, Ebner F, et al. Transient global amnesia: diffusion-weighted imaging lesions and cerebrovascular disease. Stroke 2008; 39: 2219-2225.
18. Bartsch T, Deuschl G. Transient global amnesia: functional anatomy and clinical implications. Lancet Neurol 2010; 9: 205-214.
19. Zhu L, Saito N, Abe O, Okubo T, Yamada H, Kawahara N, et al. Changes in the apparent diffusion coefficient of water and T2 relaxation time in gerbil hippocampus after mild ischemia. Neuroreport 2000; 11: 3333-3336.
20. Shepherd TM, Thelwall PE, Blackband SJ, Pike BR, Hayes RL, Wirth ED 3rd. Diffusion magnetic resonance imaging study of a rat hippocampal slice model for acute brain injury. J Cereb Blood Flow Metab 2003; 23: 1461-1470.
21. Nikonenko AG, Radenovic L, Andjus PR, Skibo GG. Structural features of ischemic damage in the hippocampus. Anat Rec 2009; 292: 1914-1921.
22. Harry GJ, Lefebvre d'Hellencourt C. Dentate gyrus: alterations that occur with hippocampal injury. Neurotoxicology 2003; 24: 343-356.
23. Avignone E, Frenguelli BG, Irving AJ. 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.
24. Bonde C, Noraberg J, Noer H, Zimmer J. Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures. Neuroscience 2005; 136: 779-794.
25. Butler TR, Self RL, Smith KJ, Sharrett-Field LJ, Berry JN, Littleton JM, et al. 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.
26. Lalonde CC, Mielke JG. Selective vulnerability of hippocampal sub-fields to oxygen-glucose deprivation is a function of animal age. Brain Res 2014; 1543: 271-279.
27. Wang X, Pal R, Chen XW, Limpeanchob N, Kumar KN, Michaelis EK. High intrinsic oxidative stress may underlie selective vulnerability of the hippocampal CA1 region. Brain Res Mol Brain Res 2005; 140: 120-126.
28. Bao X, Pal R, Hascup KN, Wang Y, Wang WT, Xu W, et al. Transgenic expression of Glud1 (glutamate dehydrogenase 1) in neurons: in vivo model of enhanced glutamate release, altered synaptic plasticity, and selective neuronal vulnerability. J Neurosci 2009; 29: 13929-13944.
29. Wang X, Zaidi A, Pal R, Garrett AS, Braceras R, Chen XW, et al. Genomic and biochemical approaches in the discovery of mechanisms for selective neuronal vulnerability to oxidative stress. BMC Neurosci 2009; 10: 12.
30. Engelhorn T, Weise J, Hammen T, Bluemcke I, Hufnagel A, Doerfler A. Early diffusion-weighted MRI predicts regional neuronal damage in generalized status epilepticus in rats treated with diazepam. Neurosci Lett 2007; 417: 275-280.
31. Fujikawa DG. The temporal evolution of neuronal damage from pilocarpineinduced status epilepticus. Brain Res 1996; 725: 11-22.
32. Wieshmann UC, Symms MR, Shorvon SD. Diffusion changes in status epilepticus. Lancet 1997; 350: 493-494.
33. Yu JT, Tan L. Diffusion-weighted magnetic resonance imaging demonstrates parenchymal pathophysiological changes in epilepsy. Brain Res Rev 2008; 59: 34-41.
34. Wall CJ, Kendall EJ, Obenaus A. Rapid alterations in diffusion-weighted images with anatomic correlates in a rodent model of status epilepticus. AJNR Am J Neuroradiol 2000; 21: 1841-1852.
35. Di Bonaventura C, Bonini F, Fattouch J, Mari F, Petrucci S, Carni M, et al. Diffusionweighted magnetic resonance imaging in patients with partial status epilepticus. Epilepsia 2009; 50: 45-52.
36. Gong G, Shi F, Concha L, Beaulieu C, Gross DW. Insights into the sequence of structural consequences of convulsive status epilepticus: a longitudinal MRI study. Epilepsia 2008; 49: 1941-1945.
37. Finke C, Kopp UA, Scheel M, Pech LM, Soemmer C, Schlichting J, et al. Functional and structural brain changes in anti-N-methyl-D-Aspartate receptor encephalitis. Ann Neurol 2013; 74: 284-296.
38. McCabe K, Tyler K, Tanabe J. Diffusion-weighted MRI abnormalities as a clue to the diagnosis of herpes simplex encephalitis. Neurology 2003; 61: 1015-1016.
39. 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.
40. Siesjo BK, Wieloch T. Epileptic brain damage: pathophysiology and neurochemical pathology. Adv Neurol 1986; 44: 813-847.
41. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011; 12: 585-601.