Direct visualization of the perforant pathway in the human brain with ex vivo diffusion tensor imaging

Frontiers in Human Neuroscience

Volumn 4, Issue , 2010, Pages

  Augustinack, Jean C ^a   Helmer, Karl ^a   Huber, Kristen E ^a   Kakunoori, Sita ^a   Zöllei, Lilla ^a,b   Fischl, Bruce ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Dentate gyrus; Entorhinal cortex; Hippocampus; Presubiculum; Resolution; Subiculum

Indexed keywords

GADOLINIUM; MYELIN;

AGED; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; DENTATE GYRUS; DIFFUSION TENSOR IMAGING; EX VIVO STUDY; FEMALE; HIGH RESOLUTION STRUCTURAL NUCLEAR MAGNETIC RESONANCE IMAGING; HISTOLOGY; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; MALE; NEUROANATOMY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PERFORANT NERVE TRACT; SIGNAL NOISE RATIO; SUBICULUM; TEMPORAL LOBE;

EID: 79953018186     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2010.00042     Document Type: Article

References (70)

1. Aggleton, J. P., Vann, S. D., and Saunders, R. C. (2005). Projections from the hippocampal region to the mammillary bodies in macaque monkeys. Eur. J. Neurosci. 22, 2519-2530.
2. Arnold, S. E., Hyman, B. T., Flory, J., Damasio, A. R., and Van Hoesen, G. W. (1991). The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb. Cortex 1, 103-116.
3. Arriagada, P. V., Marzloff, K., and Hyman, B. T. (1992). Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 42, 1681-1688.
4. Augustinack, J. C., van der Kouwe, A. J., Blackwell, M. L., Salat, D. H., Wiggins, C. J., Frosch, M. P., Wiggins, G. C., Potthast, A., Wald, L. L., and Fischl, B. R. (2005). Detection of entorhinal layer II using 7Tesla [corrected] magnetic resonance imaging. Ann. Neurol. 57, 489-494.
5. Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., Barker, G. J., Sillery, E. L., Sheehan, K., Ciccarelli, O., Thompson, A. J., Brady, J. M., and Matthews, P. M. (2003a). Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6, 750-757.
6. Behrens, T. E., Woolrich, M. W., Jenkinson, M., Johansen-Berg, H., Nunes, R. G., Clare, S., Matthews, P. M., Brady, J. M., and Smith, S. M. (2003b). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50, 1077-1088.
7. Blackstad, T. W. (1958). On the termination of some afferents to the hippocampus and fascia dentata; an experimental study in the rat. Acta Anat. (Basel) 35, 202-214.
8. Blackstad, T. W., Brink, K., Hem, J., and Jeune, B. (1970). Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J. Comp. Neurol. 138, 433-449.
9. Braak, H., and Braak, E. (1985). On areas of transition between entorhinal allocortex and temporal isocortex in the human brain. Normal morphology and lamina-specific pathology in Alzheimer's disease. Acta Neuropathol. 68, 325-332.
10. Braak, H., and Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259.
11. Cajal, S. R. (1911). Histologie du Systeme Neureux de l'Homme et des Vertebrates. Paris: Maloine.
12. Cajal, S. R. (1955). Studies on the Cerebral Cortex. Chicago, IL: The Yearbook Publishers, Inc.
13. Chakravarty, M. M., Bertrand, G., Hodge, C. P., Sadikot, A. F., and Collins, D. L. (2006). The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 30, 359-376.
14. Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., McKinstry, R. C., Burton, H., and Raichle, M. E. (1999). Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. USA 96, 10422-10427.
15. D'Arceuil, H., and de Crespigny, A. (2007). The effects of brain tissue decomposition on diffusion tensor imaging and tractography. Neuroimage 36, 64-68.
16. Domesick, V. B. (1969). Projections from the cingulate cortex in the rat. Brain Res. 12, 296-320.
17. Fischl, B., Salat, D. H., van der Kouwe, A. J., Makris, N., Segonne, F., Quinn, B. T., and Dale, A. M. (2004). Sequence-independent segmentation of magnetic resonance images. Neuroimage 23(Suppl. 1), S69-S84.
18. Gundersen, H. J., Jensen, E. B., Kieu, K., and Nielsen, J. (1999). The efficiency of systematic sampling in stereology-reconsidered. J Microsc. 193, 199-211.
19. Hjorth-Simonsen, A. (1972). Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neurol. 146, 219-232.
20. Hjorth-Simonsen, A., and Jeune, B. (1972). Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144, 215-232.
21. Hyman, B. T., Kromer, L. J., and Van Hoesen, G. W. (1988). A direct demonstration of the perforant pathway terminal zone in Alzheimer's disease using the monoclonal antibody Alz-50. Brain Res. 450, 392-397.
22. Hyman, B. T., Van Hoesen, G. W., Damasio, A. R., and Barnes, C. L. (1984). Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225, 1168-1170.
23. Hyman, B. T., Van Hoesen, G. W., Kromer, L. J., and Damasio, A. R. (1986). Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20, 472-481.
24. Itaya, S. K., Van Hoesen, G. W., and Barnes, C. L. (1986). Anterograde transsynaptic transport of WGA-HRP in the limbic system of rat and monkey. Brain Res. 398, 397-402.
25. Jiang, H., van Zijl, P. C., Kim, J., Pearlson, G. D., and Mori, S. (2006). DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Programs Biomed. 81, 106-116.
26. Jones, E. G., and Powell, T. P. (1970). An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 793-820.
27. Kalus, P., Slotboom, J., Gallinat, J., Mahlberg, R., Cattapan-Ludewig, K., Wiest, R., Nyffeler, T., Buri, C., Federspiel, A., Kunz, D., Schroth, G., and Kiefer, C. (2006). Examining the gateway to the limbic system with diffusion tensor imaging: the perforant pathway in dementia. Neuroimage 30, 713-720.
28. Kienzler, F., Jedlicka, P., Vuksic, M., Deller, T., and Schwarzacher, S. W. (2006). Excitotoxic hippocampal neuron loss following sustained electrical stimulation of the perforant pathway in the mouse. Brain Res. 1085, 195-198.
29. Kienzler, F., Norwood, B. A., and Sloviter, R. S. (2009). Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J. Comp. Neurol. 515, 181-196.
30. Kondo, H., Lavenex, P., and Amaral, D. G. (2008). Intrinsic connections of the macaque monkey hippocampal formation: I. Dentate gyrus. J. Comp. Neurol. 511, 497-520.
31. Kondo, H., Lavenex, P., and Amaral, D. G. (2009). Intrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections. J. Comp. Neurol. 515, 349-377.
32. Leergaard, T. B., White, N. S., de Crespigny, A., Bolstad, I., D'Arceuil, H., Bjaalie, J. G., and Dale, A. M. (2010). Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS One. 5, e8595 doi: 10.1371/journal.pone.0008595.
33. Lorente de No, R. (1934). Studies on the structure of the cerebral cortex II Continuation of the study of ammonic system. J. Psychol. Neurol. 46, 113-177.
34. Lori, N. F., Akbudak, E., Shimony, J. S., Cull, T. S., Snyder, A. Z., Guillory, R. K., and Conturo, T. E., (2002). Diffusion tensor fiber tracking of human brain connectivity: aquisition methods, reliability analysis and biological results. NMR Biomed. 15, 494-515.
35. Maes, F., Collignon, A., Vandermeulen, D., Marchal, G., and Suetens, P. (1997). Multimodality image registration by maximization of mutual information. IEEE Trans. Med. Imaging 16, 187-198.
36. Medina, D., DeToledo-Morrell, L., Urresta, F., Gabrieli, J. D., Moseley, M., Fleischman, D., Bennett, D. A., Leurgans, S., Turner, D. A., and Stebbins, G. T. (2006). White matter changes in mild cognitive impairment and AD: A diffusion tensor imaging study. Neurobiol. Aging 27, 663-672.
37. Meldrum, B. S. (1993). Excitotoxicity and selective neuronal loss in epilepsy. Brain Pathol. 3, 405-412.
38. Mizutani, T., and Kashara, M. (1995). Degeneration of the intrahippocampal routes of the perforant and alvear pathways in senile dementia of Alzheimer type. Neurosci. Lett. 184, 141-144.
39. Mori, S., Kaufmann, W. E., Davatzikos, C., Stieltjes, B., Amodei, L., Fredericksen, K., Pearlson, G. D., Melhem, E. R., Solaiyappan, M., Raymond, G. V., Moser, H. W., and van Zijl, P. C. (2002). Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn. Reson. Med. 47, 215-223.
40. Pandya, D. N., Van Hoesen, G. W., and Mesulam, M. M. (1981). Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 42, 319-330.
41. Papez, J. W. (1937). A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38, 725-743.
42. Powell, T. P., and Cowan, W. M. (1954). The origin of the mamillo-thalamic tract in the rat. J. Anat. 88, 489-497.
43. Raisman, G., Cowan, W. M., and Powell, T. P. (1966). An experimental analysis of the efferent projection of the hippocampus. Brain 89, 83-108.
44. Ringman, J. M., O'Neill, J., Geschwind, D., Medina, L., Apostolova, L. G., Rodriguez, Y., Schaffer, B., Varpetian, A., Tseng, B., Ortiz, F., Fitten, J., Cummings, J. L., and Bartzokis, G. (2007). Diffusion tensor imaging in preclinical and presymptomatic carriers of familial Alzheimer's disease mutations. Brain 130, 1767-1776.
45. Rose, S. E., Chen, F., Chalk, J. B., Zelaya, F. O., Strugnell, W. E., Benson, M., Semple, J., and Doddrell, D. M. (2000). Loss of connectivity in Alzheimer's disease: an evaluation of white matter tract integrity with colour coded MR diffusion tensor imaging. J. Neurol. Neurosurg. Psychiatry 69, 528-530.
46. Rosene, D. L., and Van Hoesen, G. W. (1987). ''The hippocampal formation of the primate brain: A review of some comparative aspects of cytoarchitecture and connections,'' in Cerebral Cortex. Further Aspects of Cortical Function, Including Hippocampus, Vol. 6, eds E. G. Jones and A. Peters (Plenum Press, New York), 345-456.
47. Rueckert, D., Sonoda, L. I., Hayes, C., Hill, D. L., Leach, M. O., and Hawkes, D. J. (1999). Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 18, 712-721.
48. Salat, D. H., Tuch, D. S., van der Kouwe, A. J., Greve, D. N., Pappu, V., Lee, S. Y., Hevelone, N. D., Zaleta, A. K., Growdon, J. H., Corkin, S., Fischl, B., and Rosas, H. D. (2008). White matter pathology isolates the hippocampal formation in Alzheimer's disease. Neurobiol. Aging 31, 244-256.
49. Saunders, R. C., Mishkin, M., and Aggleton, J. P. (2005). Projections from the entorhinal cortex, perirhinal cortex, presubiculum, and parasubiculum to the medial thalamus in macaque monkeys: identifying different pathways using disconnection techniques. Exp. Brain Res. 167, 1-16.
50. Saunders, R. C., and Rosene, D. L. (1988). A comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: I. Convergence in the entorhinal, prorhinal, and perirhinal cortices. J. Comp. Neurol. 271, 153-184.
51. Shepherd, T. M., Ozarslan, E., Yachnis, A. T., King, M. A., and Blackband, S. J. (2007). Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. AJNR Am. J. Neuroradiol. 28, 958-964.
52. Shimony, J. S., McKinstry, R. C., Akbudak, E., Aronovitz, J. A., Snyder, A. Z., Lori, N. F., Cull, T. S., and Conturo, T. E. (1999). Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology 212, 770-784.
53. Shipley, M. T. (1974). Presubiculum afferents to the entorhinal area and the Papez circuit. Brain Res. 67, 162-168.
54. Sloviter, R. S. (1983). ''Epileptic'' brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res. Bull. 10, 675-697.
55. Steward, O., and Scoville, S. A. (1976). Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169, 347-370.
56. Sun, S. W., Song, S. K., Harms, M. P., Lin, S. J., Holtzman, D. M., Merchant, K. M., and Kotyk, J. J. (2005). Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging. Exp. Neurol. 191, 77-85.
57. Swanson, L. W., and Cowan, W. M. (1977). An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172, 49-84.
58. Swanson, L. W., Wyss, J. M., and Cowan, W. M. (1978). An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J. Comp. Neurol. 181, 681-715.
59. Takeda, T., Uchihara, T., Mochizuki, Y., Mizutani, T., and Iwata, M. (2007). Memory deficits in amyotrophic lateral sclerosis patients with dementia and degeneration of the perforant pathway A clinicopathological study. J. Neurol. Sci. 260, 225-230.
60. Van Hoesen, G. W., and Pandya, D. N. (1975). Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res. 95, 39-59.
61. Van Hoesen, G. W., Pandya, D. N., and Butters, N. (1972). Cortical afferents to the entorhinal cortex of the Rhesus monkey. Science 175, 1471-1473.
62. Vann, S. D., Saunders, R. C., and Aggleton, J. P. (2007). Distinct, parallel path conways link the medial mammillary bodies to the anterior thalamus in macaque monkeys. Eur. J. Neurosci. 26, 1575-1586.
63. Vogt, B. A., and Pandya, D. N. (1987). Cingulate cortex of the rhesus monkey: II. Cortical afferents. J. Comp. Neurol. 262, 271-289.
64. Vogt, B. A., Rosene, D. L., and Pandya, D. N. (1979). Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey. Science 204, 205-207.
65. Wells, W. M., Viola, P., Atsumi, H., Nakajima, S., and Kikinis, R. (1996). Multi-modal volume registration by maximization of mutual information. Med. Image Anal. 1, 35-52.
66. West, M. J., Slomianka, L., and Gundersen, H. J. (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482-497.
67. Widjaja, E., Wei, X., Vidarsson, L., Moineddin, R., Macgowan, C. K., and Nilsson, D. (2009). Alteration of diffusion tensor parameters in postmortem brain. Magn. Reson. Imaging 27, 865-870.
68. Witter, M. P., and Amaral, D. G. (1991). Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J. Comp. Neurol. 307, 437-459.
69. Witter, M. P., Van Hoesen, G. W., and Amaral, D. G. (1989). Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9, 216-228.
70. Zhang, W., Olivi, A., Hertig, S. J., van Zijl, P., and Mori, S. (2008). Automated fiber tracking of human brain white matter using diffusion tensor imaging. Neuroimage 42, 771-777.