Maintenance of inhibitory interneurons and boutons in sensorimotor cortex between middle and old age in Fischer 344 X Brown Norway rats

Journal of Chemical Neuroanatomy

Volumn 32, Issue 1, 2006, Pages 46-53

  Shi, Lei ^a   Pang, Hui ^a   Linville, Martha Constance ^a   Bartley, Angela Nicole ^a   Argenta, Anne Elizabeth ^a   Brunso Bechtold, Judy Karen ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

Author keywords

Aging; GABA; Glutamic acid decarboxylase; Inhibition; Parvalbumin; Stereological quantification; Synapses

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE ANTIBODY; NUCLEAR PROTEIN; PARVALBUMIN; PROTEIN ANTIBODY;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MALE; MOLECULAR STABILITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; SENSORIMOTOR CORTEX;

AGING; ANIMALS; CEREBRAL CORTEX; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PARVALBUMINS; PRESYNAPTIC TERMINALS; RATS; RATS, INBRED BN; RATS, INBRED F344;

EID: 33747167071     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2006.04.001     Document Type: Article

References (63)

1. Abdulla F.A., Abu-Bakra M.A., Calaminici M.R., Stephenson J.D., and Sinden J.D. Importance of forebrain cholinergic and GABAergic systems to the age-related deficits in water maze performance of rats. Neurobiol. Aging 16 (1995) 41-52
2. Auerbach J.M., and Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J. Neurosci. 17 (1997) 8695-8701
3. Bacci A., Rudolph U., Huguenard J.R., and Prince D.A. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J. Neurosci. 23 (2003) 9664-9674
4. Barnes C.A. Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 17 (1994) 13-18
5. Beaulieu C. Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res. 609 (1993) 284-292
6. Bernstein D., Olton D.S., Ingram D.K., Waller S.B., Reynolds M.A., and London E.D. Radial maze performance in young and aged mice: neurochemical correlates. Pharmacol. Biochem. Behav. 22 (1985) 301-307
7. Brunso-Bechtold J.K., Linville M.C., and Sonntag W.E. Age-related synaptic changes in sensorimotor cortex of the Brown Norway X Fischer 344 rat. Brain Res. 872 (2000) 125-133
8. Celio M.R. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231 (1986) 995-997
9. DeFelipe J. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb. Cortex 3 (1993) 273-289
10. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can. J. Physiol. Pharmacol. 75 (1997) 535-545
11. Erickson S.L., and Lewis D.A. Postnatal development of parvalbumin- and GABA transporter-immunoreactive axon terminals in monkey prefrontal cortex. J. Comp. Neurol. 448 (2002) 186-202
12. Erlander M.G., Tillakaratne N.J., Feldblum S., Patel N., and Tobin A.J. Two genes encode distinct glutamate decarboxylases. Neuron 7 (1991) 91-100
13. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., and Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14 (1994) 1834-1855
14. Foster T.C. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res. Brain Res. Rev. 30 (1999) 236-249
15. Foster T.C., and Norris C.M. Age-associated changes in Ca(2+)-dependent processes: relation to hippocampal synaptic plasticity. Hippocampus 7 (1997) 602-612
16. Freund T.F. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 26 (2003) 489-495
17. Freund T.F., and Meskenaite V. Gamma-aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 738-742
18. Frick K.M., Burlingame L.A., Delaney S.S., and Berger-Sweeney J. Sex differences in neurochemical markers that correlate with behavior in aging mice. Neurobiol. Aging 23 (2002) 145-158
19. Fukuda T., Aika Y., Heizmann C.W., and Kosaka T. GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreactivities against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: a digitized quantitative analysis. J. Comp. Neurol. 395 (1998) 177-194
20. Fukuda T., and Kosaka T. The dual network of GABAergic interneurons linked by both chemical and electrical synapses: a possible infrastructure of the cerebral cortex. Neurosci. Res. 38 (2000) 123-130
21. Garraghty P.E., LaChica E.A., and Kaas J.H. Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining. Somatosens. Mot. Res. 8 (1991) 347-354
22. Geinisman Y., Detoledo-Morrell L., Morrell F., and Heller R.E. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog. Neurobiol. 45 (1995) 223-252
23. Geinisman Y., Toledo-Morrell L., Morrell F., Persina I.S., and Rossi M. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 2 (1992) 437-444
24. Giardino L., Zanni M., Fernandez M., Battaglia A., Pignataro O., and Calza L. Plasticity of GABA(a) system during ageing: focus on vestibular compensation and possible pharmacological intervention. Brain Res. 929 (2002) 76-86
25. Gonchar Y., and Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7 (1997) 347-358
26. Gonchar Y., Turney S., Price J.L., and Burkhalter A. Axo-axonic synapses formed by somatostatin-expressing GABAergic neurons in rat and monkey visual cortex. J. Comp. Neurol. 443 (2002) 1-14
27. Gulyas A.I., Megias M., Emri Z., and Freund T.F. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19 (1999) 10082-10097
28. Helfert R.H., Sommer T.J., Meeks J., Hofstetter P., and Hughes L.F. Age-related synaptic changes in the central nucleus of the inferior colliculus of Fischer-344 rats. J. Comp. Neurol. 406 (1999) 285-298
29. Jimenez-Capdeville M.E., Dykes R.W., and Myasnikov A.A. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences. J. Comp. Neurol. 381 (1997) 53-67
30. Karube F., Kubota Y., and Kawaguchi Y. Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J. Neurosci. 24 (2004) 2853-2865
31. Kaufman D.L., Houser C.R., and Tobin A.J. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 56 (1991) 720-723
32. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15 (1995) 2638-2655
33. Kawaguchi Y., and Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7 (1997) 476-486
34. Kawaguchi Y., and Kubota Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85 (1998) 677-701
35. Ling L.L., Hughes L.F., and Caspary D.M. Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 132 (2005) 1103-1113
36. Manns I.D., Alonso A., and Jones B.E. Discharge profiles of juxtacellularly labeled and immunohistochemically identified GABAergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci. 20 (2000) 9252-9263
37. Marczynski T.J. GABAergic deafferentation hypothesis of brain aging and Alzheimer's disease revisited. Brain Res. Bull. 45 (1998) 341-379
38. Mason G.F., Martin D.L., Martin S.B., Manor D., Sibson N.R., Patel A., Rothman D.L., and Behar K.L. Decrease in GABA synthesis rate in rat cortex following GABA-transaminase inhibition correlates with the decrease in GAD(67) protein. Brain Res. 914 (2001) 81-91
39. McBain C.J., and Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2 (2001) 11-23
40. Meinecke D.L., and Peters A. GABA immunoreactive neurons in rat visual cortex. J. Comp. Neurol. 261 (1987) 388-404
41. Melchitzky D.S., Sesack S.R., and Lewis D.A. Parvalbumin-immunoreactive axon terminals in macaque monkey and human prefrontal cortex: laminar, regional, and target specificity of type I and type II synapses. J. Comp. Neurol. 408 (1999) 11-22
42. Micheva K.D., and Beaulieu C. Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA-immunoreactive neurons in the rat barrel field cortex. J. Comp. Neurol. 361 (1995) 574-584
43. Micheva K.D., and Beaulieu C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J. Comp. Neurol. 373 (1996) 340-354
44. Miettinen M., Koivisto E., Riekkinen P., and Miettinen R. Coexistence of parvalbumin and GABA in nonpyramidal neurons of the rat entorhinal cortex. Brain Res. 706 (1996) 113-122
45. Miettinen R., Sirvio J., Riekkinen Sr. P., Laakso M.P., Riekkinen M., and Riekkinen Jr. P. Neocortical, hippocampal and septal parvalbumin- and somatostatin-containing neurons in young and aged rats: correlation with passive avoidance and water maze performance. Neuroscience 53 (1993) 367-378
46. Milbrandt J.C., Hunter C., and Caspary D.M. Alterations of GABAA receptor subunit mRNA levels in the aging Fischer 344 rat inferior colliculus. J. Comp. Neurol. 379 (1997) 455-465
47. Miles R., Toth K., Gulyas A.I., Hajos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
48. Owens D.F., and Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat. Rev. Neurosci. 3 (2002) 715-727
49. Peters A., and Palay S.L. The morphology of synapses. J. Neurocytol. 25 (1996) 687-700
50. Poe B.H., Linville C., and 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
51. Ren J.Q., Aika Y., Heizmann C.W., and Kosaka T. Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp. Brain Res. 92 (1992) 1-14
52. Ribak C.E., and Roberts R.C. GABAergic synapses in the brain identified with antisera to GABA and its synthesizing enzyme, glutamate decarboxylase. J. Electron. Microsc. Tech. 15 (1990) 34-48
53. Rosenzweig E.S., and Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 69 (2003) 143-179
54. Sachdev R.N., Sellien H., and Ebner F.F. Direct inhibition evoked by whisker stimulation in somatic sensory (SI) barrel field cortex of the awake rat. J. Neurophysiol. 84 (2000) 1497-1504
55. Schmitz C. Variation of fractionator estimates and its prediction. Anat. Embryol. (Berl) 198 (1998) 371-397
56. Shetty A.K., and Turner D.A. Hippocampal interneurons expressing glutamic acid decarboxylase and calcium-binding proteins decrease with aging in Fischer 344 rats. J. Comp. Neurol. 394 (1998) 252-269
57. Smith M.L., and Booze R.M. Cholinergic and GABAergic neurons in the nucleus basalis region of young and aged rats. Neuroscience 67 (1995) 679-688
58. Smith T.D., Adams M.M., Gallagher M., Morrison J.H., and Rapp P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J. Neurosci. 20 (2000) 6587-6593
59. Somogyi P., Freund T.F., Hodgson A.J., Somogyi J., Beroukas D., and Chubb I.W. Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res. 332 (1985) 143-149
60. Tombaugh G.C., Rowe W.B., Chow A.R., Michael T.H., and Rose G.M. Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats. J. Neurosci. 22 (2002) 9932-9940
61. Waller S.B., Ingram D.K., Reynolds M.A., and London E.D. Age and strain comparisons of neurotransmitter synthetic enzyme activities in the mouse. J. Neurochem. 41 (1983) 1421-1428
62. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
63. Zilles K. The cortex of the rat: a stereotaxic atlas (1985), Academic Press, Berlin