Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex

Neuroscience

Volumn 125, Issue 1, 2004, Pages 277-288

  Luebke, J I ^a   Chang, Y M ^a   Moore, T L ^a   Rosene, D L ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

( ) 2 amino 5 phosphonopentanoic acid; APV; Area 46; Bicuculline methiodide; BMI; CII; Cognitive Impairment Index; Conceptual Set Shifting Task; CSST; DNMS; Excitatory postsynaptic currents; in vitro slice; Whole cell patch clamp

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMATE RECEPTOR;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLOR VISION; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; MEMORY DISORDER; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC INHIBITION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RHESUS MONKEY; SENESCENCE; SIGNAL TRANSDUCTION; SYNAPTIC EFFICACY; TIME;

AGING; ANIMALS; COGNITION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MACACA MULATTA; MALE; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 1642421135     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.01.035     Document Type: Article

References (43)

1. Angulo M.C., Lambolez B., Audinat E., Hestrin S., Rossier J. Subunit composition, kinetic and permeation properties of AMPA receptors in single neocortical nonpyramidal cells. J Neurosci. 17:1997;6685-6696.
2. Bartzokis G., Beckson M., Lu P.H., Nuechterlein K.H., Edwards N., Mintz J. Age-related changes in frontal and temporal lobe volumes in men A magnetic resonance imaging study. Arch Gen Psychiatry. 58:2001;461-465.
3. Cahn-Weiner D.A., Malloy P.F., Boyle P.A., Marran M., Salloway S. Prediction of functional status from neuropsychological tests in community-dwelling elderly individuals. Clin Neuropsychol. 14:2000;187-195.
4. Chen K.S., Masliah E., Mallory M., Gage F.H. Synaptic loss in cognitively impaired aged rats is ameliorated by chronic human nerve growth factor infusion. Neuroscience. 68:1995;19-27.
5. de Brabander J.M., Kramers R.J., Uylings H.B. Layer specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex. Eur J Neurosci. 10:1998;1261-1269.
6. Duan H., Wearne S.L., Rocher A.B., Macedo A., Morrison J.H., Hof P.R. Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex. 19:2003;950-961.
7. Edwards F.A., Konnerth A., Sakmann B., Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch. 414:1989;600-612.
8. Fristoe N.M., Salthouse T.A., Woodard J.L. Examination of age-related deficits on the Wisconsin Card Sorting Test. Neuropsychology. 11:1997;428-436.
9. Fuster J.M. The prefrontal cortex Anatomy, physiology and neuropsychology of the frontal lobe, 3rd edition. 1997;Lippincott-Raven Publishers, New York.
10. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15:1995;193-204.
11. Herndon J.G., Moss M.B., Rosene D.L., Killiany R.J. Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res. 87:1997;25-35.
12. Hof P.R., Duan H., Page T.L., Einstein M., Wicinski B., He Y., Erwin J.M., Morrison J.H. Age-related changes in GluR2 and NMDAR1 glutamate receptor subunit protein immunoreactivity in corticocortically projecting neurons in macaque and patas monkeys. Brain Res. 928:2002;175-186.
13. Horikawa K., Armstrong W.E. A versatile means of intracellular labeling Injection of biocytin and its detection with avidin conjugates. J Neurosci Methods. 25:1988;1-11.
14. Jacobs B., Driscoll L., Schall M. Age-related dendritic and spine changes in areas 10 and 18 of human cortex A quantitative golgi study. J Comp Neurol. 386:1997;661-680.
15. Lai Z.C., Moss M.B., Killiany R.J., Rosene D.L., Herndon J.G. Executive system dysfunction in the aged monkey Spatial and object reversal learning. Neurobiol Aging. 16:1995;947-954.
16. Luebke JI, Chang YM, Mangiamele L, Rosene DL (2002) Electrophysiological and morphological properties of layer 2/3 pyramidal cells in Area 46 of the aged rhesus monkey. Soc Neurosci Abstr 1:94.8.
17. Luebke J.I., Rosene D.L. Aging alters dendritic morphology, input resistance, and inhibitory signaling in dentate granule cells of the rhesus monkey. J Comp Neurol. 460:2003;573-584.
18. Magnotta V.A., Andreasen N.C., Schultz S.K., Harris G., Cizaldo T., Heckel D. Quantitative in vivo measurement of gyrification in the human brain Changes associated with aging. Cereb Cortex. 9:1999;151-160.
19. Mhatre M.C., Ticku M.K. Aging related alterations in GABAA receptor subunit mRNA levels in Fisher rats. Mol Brain Res. 14:1992;71-78.
20. Milner B. Aspects of human frontal lobe function. Adv Neurol. 66:1995;67-81.
21. Moore TL, Killiany RJ, Rosene DL, Moss MB (2001) Lesions of dorsal prefrontal cortex produce an executive function deficit in the rhesus monkeys. Soc Neurosci Abstr.
22. Moore T.L., Killiany R.J., Herndon J.G., Rosene D.L., Moss M.B. Impairment in abstraction and set shifting in aged rhesus monkeys. Neurobiol Aging. 24:2003;125-134.
23. Morrison J.H., Hof P.R. Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer's disease. Prog Brain Res. 136:2002;467-486.
24. Moss M.B., Killiany R.J., Lai C., Rosene D.L., Herndon J.G. Recognition memory span in rhesus monkeys of advanced age. Neurobiol Aging. 18:1997;13-19.
25. O'Brien S., Rosene D.L., Luebke J.I. GABAA receptor-mediated neurotransmission in the dentate gyrus of the rhesus monkey Comparison with the rat. Synapse. 49:2003;287-289.
26. Page T.L., Einstein M., Duan H., He Y., Flores T., Rolshud D., Erwin J.M., Wearne S.L., Morrison J.H., Hof P.R. Morphological alterations in neurons forming corticocortical projections in the neocortex of aged Patas monkeys. Neurosci Lett. 317:2002;37-41.
27. Peters A. Structural changes that occur during normal aging of primate cerebral hemispheres. Neurosci Biobehav Rev. 26:2002;733-741.
28. Peters A. The effects of normal aging on myelin and nerve fibers A review. J Neurocytol. 31:2002;581-593.
29. Peters A., Leahu D., Moss M.B., McNally K.J. The effects of aging on area 46 of the frontal cortex of the rhesus monkey. Cereb Cortex. 4:1994;621-635.
30. Peters A., Morrison J.H., Rosene D.L., Hyman B.T. Are neurons lost from the primate cerebral cortex during normal aging? Cereb Cortex. 8:1998;295-300.
31. Petrides M. The role of the mid-dorsolateral prefrontal cortex in working memory. Exp Brain Res. 133:2000;44-54.
32. Petrides M. Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. J Neurosci. 20:2000;7496-7503.
33. Poe B.H., Linville C., Brunso-Bechtold J. Age-related decline of presumptive inhibitory synapses in the sensorimotor cortex as revealed by the physical disector. J Comp Neurol. 439:2001;65-72.
34. A agonist binding in aged rat hippocampus. Neurobiol Aging. 15:1994;629-633.
35. Rabbitt P., Lowe C. Patterns of cognitive ageing. Psychol Res. 63:2000;308-316.
36. Royall D.R. Executive cognitive impairment A novel perspective on dementia. Neuroepidemiology. 19:2000;293-299.
37. Rosene D.L., Nicholson T.J. Neurotransmitter receptor changes in the hippocampus and cerebral cortex in normal aging. Jones E.G., Peters A., Morrison J.H. Cerebral cortex Vol. 14. 1999;111-128 Plenum Press, New York.
38. Souchay C., Isingrini M., Espagnet L. Aging, episodic memory feeling-of-knowing, and frontal functioning. Neuropsychology. 14:2000;299-309.
39. St. John J.L., Rosene D.L., Luebke J.I. Morphology and electrophysiology of dentate granule cells in the rhesus monkey Comparison with the rat. J Comp Neurol. 387:1997;136-147.
40. Swanson G.T., Kamboj S.K., Cull-Candy S.G. Single channel properties of recombinant AMPA receptors depend on RNA editing, splice variation and subunit composition. J Neurosci. 17:1997;58-69.
41. Tigges J., Herndon J.G., Peters A. Axon terminals on Betz cell somata of area 4 in rhesus monkey throughout adulthood. Anat Rec. 232:1992;305-315.
42. Wong T.P., Campbell P.M., Ribiero-da-silva A., Cuello A.C. Synaptic numbers across cortical laminae and cognitive performance of the rat during aging. Neuroscience. 84:1998;403-412.
43. Wong T.P., Marchese G., Casu M.A., Roberto-da-Silva A., Cuello A.C., De Koninck Y. Loss of presynaptic and postsynaptic structures is accompanied by compensatory increase in action potential-dependent synaptic input to layer V neocortical pyramicdal meurons in aged rats. J Neurosci. 20:2000;8596-8606.