Hippocampal and diencephalic pathology in developmental amnesia

Cortex

Volumn 86, Issue , 2017, Pages 33-44

  Dzieciol, Anna M ^a   Bachevalier, Jocelyne ^b   Saleem, Kadharbatcha S ^c   Gadian, David G ^a   Saunders, Richard ^c   Chong, W K Kling ^d   Banks, Tina ^d   Mishkin, Mortimer ^c   Vargha Khadem, Faraneh ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b EMORY UNIVERSITY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

Hippocampus; Hypoxia ischaemia; Mammillary bodies; Memory; Thalamus

Indexed keywords

ADOLESCENT; ADULT; AMNESIA; ARTICLE; BRAIN ATROPHY; BRAIN DAMAGE; BRAIN SIZE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL AMNESIA; DIENCEPHALON; FEMALE; HIPPOCAMPUS; HUMAN; MALE; MAMMILLARY BODY; NEUROIMAGING; NEUROPSYCHOLOGY; THALAMUS; VISUAL MEMORY; ATROPHY; DIAGNOSTIC IMAGING; EPISODIC MEMORY; PATHOLOGY; SHORT TERM MEMORY; YOUNG ADULT;

ADOLESCENT; ADULT; AMNESIA; ATROPHY; CHILD; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MAMMILLARY BODIES; MEMORY, EPISODIC; MEMORY, SHORT-TERM; YOUNG ADULT;

EID: 84997343327     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2016.09.016     Document Type: Article

References (68)

1. Adlam, A.-L.R., Malloy, M., Mishkin, M., Vargha-Khadem, F., Dissociation between recognition and recall in developmental amnesia. Neuropsychologia 47:11 (2009), 2207–2210.
2. Adlam, A.-L.R., Vargha-Khadem, F., Mishkin, M., de Haan, M., Deferred imitation of action sequences in developmental amnesia. Journal of Cognitive Neuroscience 17:2 (2005), 240–248.
3. Aggleton, J.P., O'Mara, S.M., Vann, S.D., Wright, N.F., Tsanov, M., Erichsen, J.T., Hippocampal-anterior thalamic pathways for memory: Uncovering a network of direct and indirect actions. The European Journal of Neuroscience 31:12 (2010), 2292–2307.
4. Aggleton, J.P., Vann, S.D., Saunders, R.C., Projections from the hippocampal region to the mammillary bodies in macaque monkeys. The European Journal of Neuroscience 22:10 (2005), 2519–2530.
5. Bachevalier, J., Meunier, M., Cerebral ischemia: Are the memory deficits associated with hippocampal cell loss?. Hippocampus 6:5 (1996), 553–560.
6. Baddeley, A.D., Emslie, H., Nimmo-Smith, I., Doors and people: A re-analysis of psychometric data. 1994, Thames Valley Test Co, Bury St. Edmunds, UK.
7. Bleier, R., Retrograde transsynaptic cellular degeneration in mammillary and ventral tegmental nuclei following limbic decortication in rabbits of various ages. Brain Research 15:2 (1969), 365–393.
8. Caine, D., Watson, J.D., Neuropsychological and neuropathological sequelae of cerebral anoxia: A critical review. Journal of the International Neuropsychological Society 6:1 (2000), 86–99.
9. Caulo, M., Van Hecke, J., Toma, L., Ferretti, A., Tartaro, A., Colosimo, C., et al. Functional MRI study of diencephalic amnesia in Wernicke-Korsakoff syndrome. Brain 128:Pt 7 (2005), 1584–1594.
10. Chao, C.P., Zaleski, C.G., Patton, A.C., Neonatal hypoxic-ischemic encephalopathy: Multimodality imaging findings. Radiographics 26:Suppl. 1 (2006), S159–S172.
11. Chiaravalloti, N.D., Tulsky, D.S., Glosser, G., Validation of the WMS-III Facial Memory subtest with the Graduate Hospital Facial Memory Test in a sample of right and left anterior temporal lobectomy patients. Journal of Clinical and Experimental Neuropsychology 26:4 (2004), 484–497.
12. Cipolotti, L., Husain, M., Crinion, J., Bird, C.M., Khan, S.S., Losseff, N., et al. The role of the thalamus in amnesia: A tractography, high-resolution MRI and neuropsychological study. Neuropsychologia 46:11 (2008), 2745–2758.
13. Cohen, M., Children's memory scale. 1997, Harcourt Brace & Company, San Antonio (TX).
14. Cooper, J.M., Gadian, D.G., Jentschke, S., Goldman, A., Munoz, M., Pitts, G., et al. Neonatal hypoxia, hippocampal atrophy, and memory Impairment: Evidence of a causal sequence. Cerebral Cortex 25 (2015), 1469–1476.
15. Copenhaver, B.R., Rabin, L.A., Saykin, A.J., Roth, R.M., Wishart, H.A., Flashman, L.A., et al. The fornix and mammillary bodies in older adults with Alzheimer's disease, mild cognitive impairment, and cognitive complaints: A volumetric MRI study. Psychiatry Research 147:2–3 (2006), 93–103.
16. Denby, C.E., Vann, S.D., Tsivilis, D., Aggleton, J.P., Montaldi, D., Roberts, N., et al. The frequency and extent of mammillary body atrophy associated with surgical removal of a colloid cyst. AJNR. American Journal of Neuroradiology 30:4 (2009), 736–743.
17. Di Paola, M., Caltagirone, C., Fadda, L., Sabatini, U., Serra, L., Carlesimo, G.A., Hippocampal atrophy is the critical brain change in patients with hypoxic amnesia. Hippocampus 18:7 (2008), 719–728.
18. Doss, R.C., Chelune, G.J., Naugle, R.I., WMS-III performance in epilepsy patients following temporal lobectomy. Journal of the International Neuropsychological Society : JINS 10:2 (2004), 173–179.
19. Dunn, L., Whetton, C., Pintilie, D., British picture vocabulary scale. 1982, NFER-Nelson, Windsor, Berkshire, UK.
20. Faro, M.D., Windle, W.F., Transneuronal degeneration in brains of monkeys asphyxiated at birth. Experimental Neurology 24:1 (1969), 38–53.
21. Gadian, D.G., Aicardi, J., Watkins, K.E., Porter, D.A., Mishkin, M., Vargha-Khadem, F., Developmental amnesia associated with early hypoxic-ischaemic injury. Brain 123:Pt 3 (2000), 499–507.
22. Gold, J.J., Squire, L.R., The anatomy of amnesia: Neurohistological analysis of three new cases. Learning & Memory 13:6 (2006), 699–710.
23. Guderian, S., Dzieciol, A.M., Gadian, D.G., Jentschke, S., Doeller, C.F., Burgess, N., et al. Hippocampal volume reduction in humans predicts impaired allocentric spatial memory in virtual-reality navigation. The Journal of Neuroscience 35:42 (2015), 14123–14131.
24. Harding, A., Halliday, G., Caine, D., Kril, J., Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123:Pt 1 (2000), 141–154.
25. Howard, D., Patterson, K., Pyramids and palm trees: A test of semantic access from pictures and words. 1992, Thames Valley Test Company, Bury St Edmunds, UK.
26. Hurley, N.C., Maguire, E.A., Vargha-Khadem, F., Patient HC with developmental amnesia can construct future scenarios. Neuropsychologia 49:13 (2011), 3620–3628.
27. Isaacs, E.B., Vargha-Khadem, F., Watkins, K.E., Lucas, A., Mishkin, M., Gadian, D.G., Developmental amnesia and its relationship to degree of hippocampal atrophy. Proceedings of the National Academy of Sciences of the United States of America 100:22 (2003), 13060–13063.
28. Johkura, K., Naito, M., Wernicke's encephalopathy-like lesions in global cerebral hypoxia. Journal of Clinical Neuroscience 15:3 (2008), 318–319.
29. Kodama, F., Ogawa, T., Sugihara, S., Kamba, M., Kohaya, N., Kondo, S., et al. Transneuronal degeneration in patients with temporal lobe epilepsy: Evaluation by MR imaging. European Radiology 13:9 (2003), 2180–2185.
30. Kopelman, M.D., Disorders of memory. Brain 125:Pt 10 (2002), 2152–2190.
31. Kumar, R., Birrer, B.V.X., Macey, P.M., Woo, M.A., Gupta, R.K., Yan-Go, F.L., et al. Reduced mammillary body volume in patients with obstructive sleep apnea. Neuroscience Letters 438:3 (2008), 330–334.
32. Kumar, R., Woo, M.A., Birrer, B.V.X., Macey, P.M., Fonarow, G.C., Hamilton, M.A., et al. Mammillary bodies and fornix fibers are injured in heart failure. Neurobiology of Disease 33:2 (2009), 236–242.
33. Kuwert, T., Hömberg, V., Steinmetz, H., Unverhau, S., Langen, K.J., Herzog, H., et al. Posthypoxic amnesia: Regional cerebral glucose consumption measured by positron emission tomography. Journal of the Neurological Sciences 118:1 (1993), 10–16.
34. Latchaw, R.E., Truwit, C.E., Imaging of perinatal hypoxic-ischemic brain injury. Seminars in Pediatric Neurology 2:1 (1995), 72–89.
35. Loftus, M., Knight, R.T., Amaral, D.G., An analysis of atrophy in the medial mammillary nucleus following hippocampal and fornix lesions in humans and nonhuman primates. Experimental Neurology 163:1 (2000), 180–190.
36. Low, J.A., Determining the contribution of asphyxia to brain damage in the neonate. The Journal of Obstetrics and Gynaecology Research 30:4 (2004), 276–286.
37. Magnotta, V.A., Harris, G., Andreasen, N.C., O'Leary, D.S., Yuh, W.T.C., Heckel, D., Structural MR image processing using the BRAINS2 toolbox. Computerized Medical Imaging and Graphics 26:4 (2002), 251–264.
38. Markowitsch, H.J., Weber-Luxemburger, G., Ewald, K., Kessler, J., Heiss, W.D., Patients with heart attacks are not valid models for medial temporal lobe amnesia. A neuropsychological and FDG-PET study with consequences for memory research. European Journal of Neurology 4:2 (1997), 178–184.
39. Millis, S.R., Malina, a C., Bowers, D. a, Ricker, J.H., Confirmatory factor analysis of the Wechsler memory scale-III. Journal of Clinical and Experimental Neuropsychology 21:1 (1999), 87–93.
40. Olsen, R.K., Palombo, D.J., Rabin, J.S., Levine, B., Ryan, J.D., Rosenbaum, R.S., Volumetric analysis of medial temporal lobe subregions in developmental amnesia using high-resolution magnetic resonance imaging. Hippocampus 23:10 (2013), 855–860.
41. Pan, A., Kumar, R., Macey, P.M., Fonarow, G.C., Harper, R.M., Woo, M.A., Visual assessment of brain magnetic resonance imaging detects injury to cognitive regulatory sites in patients with heart failure. Journal of Cardiac Failure 19:2 (2013), 94–100.
42. Papez, J.W., A proposed mechanism of emotion. Archives of Neurology and Psychology 38 (1937), 725–743.
43. Patai, E.Z., Gadian, D.G., Cooper, J.M., Dzieciol, A.M., Mishkin, M., Vargha-Khadem, F., Extent of hippocampal atrophy predicts degree of deficit in recall. Proceedings of the National Academy of Sciences of the United States of America 112:41 (2015), 12830–12833.
44. Patenaude, B., Smith, S.M., Kennedy, D.N., Jenkinson, M., A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage 56:3 (2011), 907–922.
45. Reed, L.J., Lasserson, D., Marsden, P., Stanhope, N., Stevens, T., Bello, F., et al. FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex 39:4–5 (2003), 1027–1045.
46. Reed, L.J., Marsden, P., Lasserson, D., Sheldon, N., Lewis, P., Stanhope, N., et al. FDG-PET analysis and findings in amnesia resulting from hypoxia. Memory 7:5–6 (1999), 599–612.
47. Rempel-Clower, N.L., Zola, S.M., Squire, L.R., Amaral, D.G., Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience 16:16 (1996), 5233–5255.
48. Rosenbaum, R.S., Carson, N., Abraham, N., Bowles, B., Kwan, D., Köhler, S., et al. Impaired event memory and recollection in a case of developmental amnesia. Neurocase 17:5 (2011), 394–409.
49. Rosenbaum, R.S., Gao, F., Honjo, K., Raybaud, C., Olsen, R.K., Palombo, D.J., et al. Congenital absence of the mammillary bodies: A novel finding in a well-studied case of developmental amnesia. Neuropsychologia 65 (2014), 82–87.
50. Saunders, R.C., Mishkin, M., Aggleton, J.P., Projections from the entorhinal cortex, perirhinal cortex, presubiculum, and parasubiculum to the medial thalamus in macaque monkeys: Identifying different pathways using disconnection techniques. Experimental Brain Research 167:1 (2005), 1–16.
51. Schmidt-Kastner, R., Freund, T.F., Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40:3 (1991), 599–636.
52. Schubert, T., Friede, R.L., Transneuronal mammillary atrophy. Journal of Neurology 221:2 (1979), 67–72.
53. Sie, L.T.L., Van Der Knaap, M.S., Oosting, J., De Vries, L.S., Lafeber, H.N., Valk, J., MR patterns of hypoxic-ischemic brain damage after prenatal, perinatal or postnatal asphyxia. Neuropediatrics 31:3 (2000), 128–136 (October 1997).
54. Spiers, H.J., Maguire, E.A., Burgess, N., Hippocampal amnesia. Neurocase 7:5 (2001), 357–382.
55. Squire, L.R., Wixted, J.T., The cognitive neuroscience of human memory since H.M. Annual Review of Neuroscience 34 (2011), 259–288.
56. Thayyil, S., Chandrasekaran, M., Taylor, A., Bainbridge, A., Cady, E.B., Chong, W.K., et al. Cerebral magnetic resonance biomarkers in neonatal encephalopathy: A meta-analysis. Pediatrics 125:2 (2010), e382–e395.
57. Tsivilis, D., Vann, S.D., Denby, C., Roberts, N., Mayes, A.R., Montaldi, D., et al. A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nature Neuroscience 11:7 (2008), 834–842.
58. Vann, S.D., Re-evaluating the role of the mammillary bodies in memory. Neuropsychologia 48:8 (2010), 2316–2327.
59. Vann, S.D., Albasser, M.M., Hippocampal, retrosplenial, and prefrontal hypoactivity in a model of diencephalic amnesia: Evidence towards an interdependent subcortical-cortical memory network. Hippocampus 19:11 (2009), 1090–1102.
60. Vann, S.D., Tsivilis, D., Denby, C.E., Quamme, J.R., Yonelinas, A.P., Aggleton, J.P., et al. Impaired recollection but spared familiarity in patients with extended hippocampal system damage revealed by 3 convergent methods. Proceedings of the National Academy of Sciences of the United States of America 106:13 (2009), 5442–5447.
61. Vargha-Khadem, F., Gadian, D.G., Watkins, K.E., Connelly, A., Van Paesschen, W., Mishkin, M., Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277:5324 (1997), 376–380.
62. Vargha-Khadem, F., Salmond, C.H., Watkins, K.E., Friston, K.J., Gadian, D.G., Mishkin, M., Developmental amnesia: Effect of age at injury. Proceedings of the National Academy of Sciences of the United States of America 100:17 (2003), 10055–10060.
63. Vortmeyer, A.O., Hagel, C., Laas, R., Hypoxia-ischemia and thiamine deficiency. Clinical Neuropathology 12:4 (1993), 184–190.
64. Wechsler, D., Wechsler memory Scale-3rd ed. 1997, The Psychological Corporation, San Antonio (TX).
65. Wechsler, D., Wechsler adult intelligence Scale-3rd ed UK (WAIS-III). 1998, The Psychological Corporation, Sidcup, Kent, UK.
66. Wechsler, D., Wechsler individual achievement Test-2nd ed. 2001, The Psychological Corporation, San Antonio (TX).
67. Wechsler, D., Wechsler Intelligence Scale for Children-4th ed (WISC-IV) administration and scoring manual. 2003, The Psychological Corporation, San Antonio (TX).
68. Wilson, B., Cockburn, J., Baddeley, A.D., The Rivermead behavioural memory test. 2nd ed., 1985, Thames Valley Test, Reading, UK.