Age-related reduction in microcolumnar structure correlates with cognitive decline in ventral but not dorsal area 46 of the rhesus monkey

Neuroscience

Volumn 158, Issue 4, 2009, Pages 1509-1520

  Cruz, L ^a   Roe, D L ^c   Urbanc, B ^a   Inglis, A ^b   Stanley, H E ^b   Rosene, D L ^c,d  

^a DREXEL UNIVERSITY   (United States)

^b Boston University   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

aging; cognition; microcolumns; minicolumns; neuronal organization; primate brain

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN; BRAIN CORTEX; BRAIN WEIGHT; CELL DENSITY; COGNITIVE DEFECT; DENDRITIC CELL; FEMALE; LEARNING; MEMORY; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RHESUS MONKEY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN MAPPING; COGNITION DISORDERS; FEMALE; MACACA MULATTA; NEURONS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX;

EID: 60149086048     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.11.033     Document Type: Article

References (68)

1. Benes F.M., and Bird E.D. An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Arch Gen Psychiatry 44 (1987) 608-616
2. Buldyrev S.V., Cruz L., Gomez-Isla T., Gomez-Tortosa E., Havlin S., Le R., Stanley H.E., Urbanc B., and Hyman B.T. Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias. Proc Natl Acad Sci U S A 97 (2000) 5039-5043
3. Buxhoeveden D.P., and Casanova M.F. The minicolumn and evolution of the brain. Brain Behav Evol 60 (2002) 125-151
4. Buxhoeveden D., and Casanova M.F. Encephalization, minicolumns, and hominid evolution. In: Casanova M.F. (Ed). Neocortical modularity and the cell minicolumn (2005), Nova Science Publishers, New York 117-136
5. Buxhoeveden D., Roy E., Switala A., and Casanova M.F. Reduced interneuronal space in schizophrenia. Biol Psychiatry 47 (2000) 681-683
6. Buxhoeveden D., Fobbs A., Roy E., and Casanova M. Quantitative comparison of radial cell columns in children with Down's syndrome and controls. J Intellect Disabil Res 46 (2002) 76-81
7. Buxhoeveden D.P., Hasselrot U., Buxhoeveden N.E., Booze R.M., and Mactutus C.F. Microanatomy in 21 day rat brains exposed prenatally to cocaine. Int J Dev Neurosci 24 (2006) 335-341
8. Casanova M.F., Buxhoeveden D.P., Cohen M., Switala A.E., and Roy E.L. Minicolumnar pathology in dyslexia. Ann Neurol 52 (2002) 108-110
9. Casanova M.F., Buxhoeveden D., and Gomez J. Disruption in the inhibitory architecture of the cell minicolumn: Implications for autism. Neuroscientist 9 (2003) 496-507
10. Chang Y.-M., Rosene D.L., Killiany R.J., Mangiamele L.A., and Luebke J.I. Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cereb Cortex 15 (2005) 409-418
11. Constantinidis C., Franowicz M.N., and Goldman-Rakic P.S. Coding specificity in cortical microcircuits: a multiple-electrode analysis of primate prefrontal cortex. J Neurosci 21 (2001) 3646-3655
12. Cruz L., Roe D.L., Urbanc B., Cabral H., Stanley H.E., and Rosene D.L. Age-related reduction in microcolumnar structure in area 46 of the rhesus monkey correlates with behavioral decline. Proc Natl Acad Sci U S A 101 (2004) 15846-15851
13. Cruz L., Buldyrev S.V., Peng S., Roe D.L., Urbanc B., Stanley H.E., and Rosene D.L. A statistically based density map method for identification and quantification of regional differences in microcolumnarity in the monkey brain. J Neurol Methods 141 (2005) 321-332
14. Cruz L., Urbanc B., Inglis A., Rosene D.L., and Stanley H.E. Generating a model of the three-dimensional spatial distribution of neurons using density maps. Neuroimage 40 (2008) 1105-1115
15. DeFelipe J., Hendry S.H.C., Hashikawa T., Molinari M., and Jones E.G. A microcolumnar structure of monkey cerebral-cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37 (1990) 655-673
16. Dickstein D.L., Kabaso D., Rocher A.B., Luebke J.I., Wearne S.L., and Hof P.R. Changes in the structural complexity of the aged brain. Aging Cell 6 (2007) 275-284
17. Duan H., Wearne S.L., Rocher A.B., Macedo A., Morrison J.H., and Hof P.R. Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13 (2003) 950-961
18. Goldman P.S., and Rosvold H.E. Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Exp Neurol 27 (1970) 291-304
19. Goldman P.S., Rosvold H.E., Vest B., and Galkin T.W. Analysis of the delayed alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkey. J Comp Physiol Psychol 77 (1971) 212-220
20. Goldman-Rakic P.S. Topography of cognition: Parallel distributed networks in primate association cortex. Annu Rev Neurosci 11 (1988) 137-156
21. Grill J.D., and Riddle D.R. Age-related and laminar-specific dendritic changes in the medial frontal cortex of the rat. Brain Res 937 (2002) 8-21
22. Helmstaedter M., de Kock C.P.J., Feldmeyer D., Bruno R.M., and Sakmann B. Reconstruction of an average cortical column in silico. Brain Res Rev 55 (2007) 193-203
23. Herndon J.G., Moss M.B., Rosene D.L., and Killiany R.J. Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 87 (1997) 25-34
24. Horton J.C., and Adams D.L. The cortical column: a structure without a function. Phil Trans R Soc B 360 (2005) 837-862
25. Hubel D.H., and Wiesel T.N. Shape and arrangement of columns in cat's striate cortex. J Physiol 165 (1963) 559-568
26. Hubel D.H., and Wiesel T.N. Anatomical demonstration of columns in the monkey striate cortex. Nature 221 (1969) 747-750
27. Hubel D.H., and Wiesel T.N. Functional architecture of macaque visual cortex. Proc R Soc Lond B 198 (1977) 1-59
28. Inglis A., Cruz L., Roe D.L., Stanley H.E., Rosene D.L., and Urbanc B. Automated retrieval of neuron location from Nissl-stained tissue. J Microsc 230 (2008) 339-347
29. Jones E.G. Microcolumns in the cerebral cortex. Proc Natl Acad Sci U S A 97 (2000) 5019-5021
30. Krieger P., Kuner T., and Sakmann B. Synaptic connections between layer 5B pyramidal neurons in mouse somatosensory cortex are independent of apical dendrite bundling. J Neurosci 27 (2007) 11473-11482
31. Lambrecht R., and LeDoux J. Structural plasticity and memory. Nat Rev Neurosci 5 (2004) 45-54
32. Leuner B., Falduto J., and Shors T. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23 (2003) 659-665
33. Leventhal A.G., Wang Y., Pu M., Zhou Y., and Ma Y. GABA and its agonists improved visual cortical function in senescent monkeys. Science 300 (2003) 812-815
34. Luebke J.I., Chang Y.-M., Moore T.L., and Rosene D.L. Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex. Neuroscience 125 (2004) 277-288
35. Lynch M.A. Long-term potentiation and memory. Physiol Rev 84 (2004) 87-136
36. Moore T.L., Killiany R.J., Herndon J.G., Rosene D.L., and Moss M.B. Impairment in abstraction and set shifting in aged rhesus monkeys. Neurobiol Aging 5717 (2002) 1-10
37. Moore T.L., Killiany R.J., Rosene D.L., Prusty S., Hollander W., and Moss M.B. Impairment of executive function induced by hypertension in the rhesus monkey (Macaca mulatta). Behav Neurosci 116 (2002) 387-396
38. Moore T.L., Killiany R.J., Herndon J.G., Rosene D.L., and Moss M.B. A non-human primate test of abstraction and set shifting: An automated adaptation of the Wisconsin Card Sorting Test. J Neurosci Methods 146 (2005) 165-173
39. Morrison J.H., and Hof P.R. Life and death of neurons in the aging cerebral cortex. Int Rev Neurobiol 81 (2007) 41-57
40. Mountcastle V.B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20 (1957) 408-434
41. Mountcastle V.B. The columnar organization of the neocortex. Brain 120 (1997) 701-722
42. Mountcastle V.B. Introduction [untitled]. Cereb Cortex 13 (2003) 2-4
43. Page T.L., Einstein M., Duan H., He Y., Flores T., Rolshud D., Erwin J.M., Wearne S.L., Morrison J.H., and Hof P.R. Morphological alterations in neurons forming corticocortical projections in the neocortex of aged Patas monkeys. Neurosci Lett 317 (2002) 37-41
44. Pakkenberg B., and Gundersen H.J.G. Neocortical neuron number in humans: Effect of sex and age. J Comp Neurol 384 (1997) 312-320
45. Pakkenberg B., Pelvig D., Marner L., Bundgaard M.J., Gundersen H.J.G., Nyengaard J.R., and Regeur L. Aging and the human neocortex. Exp Gerontol 38 (2003) 95-99
46. Peters A. The organization of the primary visual cortex in the macaque. In: Peters A., and Rockland K.S. (Eds). Cerebral cortex Vol. 10 (1994), Plenum Press, New York 1-35
47. Peters A. The effects of normal aging on myelin and nerve fibers: A review. J Neurocytol 31 (2002) 581-593
48. Peters A., and Rosene D.L. In aging, is it gray or white?. J Comp Neurol 462 (2003) 139-143
49. Peters A., and Sethares C. Myelinated axons and the pyramidal cell modules in monkey primary visual cortex. J Comp Neurol 365 (1996) 232-255
50. Peters A., Leahu D., Moss M.B., and McNally K.J. The effects of aging on area-46 of the frontal-cortex of the rhesus-monkey. Cereb Cortex 4 (1994) 621-635
51. Peters A., Morrison J.H., Rosene D.L., and Hyman B.T. Feature article: are neurons lost from the primate cerebral cortex during normal aging?. Cereb Cortex 8 (1998) 295-300
52. Petrides M., and Pandya D.N. Comparative architectonic analysis of the human and macaque frontal cortex. In: Grafman J., and Boller F. (Eds). Handbook of neuropsychology Vol. 9 (1994), Elsevier, Amsterdam 17-58
53. Petrides M. Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. J Neurosci 20 (2000) 7496-7503
54. Petrides M. The role of the mid-dorsolateral prefrontal cortex in working memory. Exp Brain Res 133 (2000) 44-54
55. Petrides M. Lateral prefrontal cortex: architectonic and functional organization. Phil Trans R Soc B 360 (2005) 781-795
56. Purves D., Riddle D.R., and LaMantia A.S. Iterated patterns of brain circuitry (or how the cortex gets its spots). Trends Neurosci 15 (1992) 362-368
57. Rockland K.S., and Ichinohe N. Some thoughts on cortical minicolumns. Exp Brain Res 158 (2004) 265-277
58. Rosene D.L., Roy N.J., and Davis B.J. A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J Histochem Cytochem 34 (1986) 1301-1315
59. Roth G.S., Mattison J.A., Ottinger M.A., Chachich M.E., Lane M.A., and Ingram D.K. Aging in rhesus monkeys: Relevance to human health interventions. Science 305 (2004) 1423-1426
60. Sandell J.H., and Peters A. Disrupted myelin and axon loss in the anterior commissure of the aged rhesus monkey. J Comp Neurol 466 (2003) 14-30
61. Schmolesky M.T., Wang Y., Pu M., and Leventhal A.G. Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys. Nat Neurosci 3 (2000) 384-390
62. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neuro-genesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-375
63. Smith D.E., Rapp P.R., McKay H.M., Roberts J.A., and Tuszynski M.H. Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. J Neurosci 24 (2004) 4373-4381
64. Swindale N.V. Is the cerebral cortex modular?. Trends Neurosci 13 (1990) 487-492
65. Tigges J., Gordon T.P., McClure J.M., Hall E.C., and Peters A. Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. Am J Primatol 15 (1988) 263-273
66. Van Hoesen G.W., and Solodkin A. Some modular features of temporal cortex in humans as revealed by pathological changes in Alzheimer's disease. Cereb Cortex 3 (1993) 465-475
67. Vercelli A.E., Garbossa D., Curtetti R., and Innocenti G.M. Somatodendritic minicolumns of output neurons in the rat visual cortex. Eur J Neurosci 20 (2004) 495-502
68. Weeks J.C. Thinking globally, acting locally: steroid hormone regulation of the dendritic architecture, synaptic connectivity and death of an individual neuron. Prog Neurobiol 70 (2003) 421-442