title: Synaptic characteristics of dentate gyrus axonal boutons and their relationships with aging, menopause, and memory in female rhesus monkeys.
abstract: Age-related memory impairment occurs in many mammalian species, including humans. Moreover, women undergoing the menopausal transition often complain of problems with memory. We recently reported that rhesus monkeys display age- and menopause-related recognition memory impairment on a hippocampus-reliant test [delayed nonmatching-to-sample (DNMS)]. In the same monkeys, perforated synapse densities in the dentate gyrus outer molecular layer (OML) correlated with DNMS recognition accuracy, while total axospinous synapse density was similar across age and menses groups. The current study examined whether synaptic characteristics of OML axonal boutons are coupled with age- or menopause-related memory deficits. Using serial section electron microscopy, we measured the frequencies of single-synapse boutons (SSBs), multiple-synapse boutons (MSBs), and boutons with no apparent synaptic contacts [nonsynaptic boutons (NSBs)] in the OML. Aged females had double the percentage of NSBs compared with young females, and this measure correlated positively and inversely with DNMS acquisition (number of trials to criterion) and delay performance (average accuracy), respectively. Aged compared with young females also had a lower frequency of MSBs and a lower number of synaptic contacts per MSB, and the latter variable inversely correlated with DNMS acquisition. Although proportions of NSBs, SSBs, and MSBs were similar across menses groups, compared with premenopausal monkeys, peri/postmenopausal monkeys had fewer MSBs contacting one or more segmented perforated synapses, and the abundance of this bouton subtype positively correlated with DNMS performance. These results suggest that age- and menopause-related shifts in OML synaptic subtypes may be coupled with deficits in task acquisition and recognition memory.
authors: Fishberg Department of Neuroscience and Kastor Neurobiology of Aging Laboratories, Mount Sinai School of Medicine, New York, New York 10029, USA.
authors: Yuko
authors: Y
authors: Hara
authors: C Sehwan
authors: CS
authors: Park
authors: William G M
authors: WG
authors: Janssen
authors: Michael
authors: M
authors: Punsoni
authors: Peter R
authors: PR
authors: Rapp
authors: John H
authors: JH
authors: Morrison
references: Brain Res. 1987 Feb 3;402(2):205-16
references: 3828793
references: Brain Res. 1987 Oct 13;423(1-2):179-88
references: 3676805
references: Science. 1997 Oct 17;278(5337):412-9
references: 9334292
references: Science. 1978 Dec 8;202(4372):1096-8
references: 715459
references: J Comp Neurol. 2004 Jul 19;475(2):238-46
references: 15211464
references: Neuroscience. 2009 Mar 17;159(2):896-907
references: 19105974
references: Acta Anat (Basel). 1996;157(1):63-72
references: 9096743
references: Biol Reprod. 2008 Sep;79(3):398-406
references: 18495681
references: Am J Primatol. 1988;15(3):263-273
references: 31968890
references: Neurobiol Aging. 1991 Sep-Oct;12(5):481-6
references: 1770984
references: J Neurosci. 1989 Jan;9(1):216-28
references: 2913203
references: Neurobiol Aging. 1988 Sep-Dec;9(5-6):495-502
references: 3062461
references: Science. 1991 Sep 20;253(5026):1380-6
references: 1896849
references: Proc Natl Acad Sci U S A. 2010 Jul 13;107(28):12687-91
references: 20616040
references: Neurobiol Aging. 1997 Sep-Oct;18(5):549-53
references: 9390783
references: Neuron. 1995 Sep;15(3):711-20
references: 7546749
references: J Neurocytol. 1974 Dec;3(6):659-75
references: 4461770
references: Acta Anat (Basel). 1995;153(1):39-48
references: 8560958
references: Proc Natl Acad Sci U S A. 1986 May;83(9):3027-31
references: 3458260
references: Science. 1984 Sep 14;225(4667):1168-70
references: 6474172
references: Z Zellforsch Mikrosk Anat. 1969 Sep 22;100(4):487-506
references: 5351190
references: Neuron. 1996 Oct;17(4):617-26
references: 8893020
references: Neurobiol Aging. 2006 Oct;27(10):1405-15
references: 16183171
references: Brain Res. 1991 Dec 6;566(1-2):77-88
references: 1814558
references: Neuron. 2009 Feb 12;61(3):340-50
references: 19217372
references: Hippocampus. 1993 Oct;3(4):435-45
references: 8269035
references: Neuron. 2000 Nov;28(2):527-36
references: 11144361
references: Neurobiol Aging. 1987 Sep-Oct;8(5):435-40
references: 3683724
references: Hippocampus. 1992 Oct;2(4):445-56
references: 1308201
references: J Neurophysiol. 1990 Jul;64(1):119-32
references: 1974917
references: J Neurosci. 1999 Nov 15;19(22):10153-63
references: 10559423
references: Nature. 1999 Nov 25;402(6760):421-5
references: 10586883
references: Trends Neurosci. 1995 Aug;18(8):365-9
references: 7482800
references: Neurobiol Aging. 2003 Jan-Feb;24(1):157-65
references: 12493561
references: Curr Opin Neurobiol. 2007 Oct;17(5):516-24
references: 17950593
references: Neuron. 2003 Dec 4;40(5):945-57
references: 14659093
references: J Neurosci. 2003 Jul 2;23(13):5708-14
references: 12843274
references: Biol Reprod. 1997 Aug;57(2):335-40
references: 9241047
references: Neurobiol Aging. 1992 Mar-Apr;13(2):283-91
references: 1522944
references: Proc Natl Acad Sci U S A. 2004 May 4;101(18):7181-6
references: 15118105
references: Biochem Biophys Res Commun. 2003 Oct 17;310(2):303-11
references: 14521910
references: J Comp Neurol. 2003 Oct 27;465(4):540-50
references: 12975814
references: J Comp Neurol. 2000 Jul 3;422(3):396-401
references: 10861515
references: J Neuropathol Exp Neurol. 1996 Aug;55(8):861-74
references: 8759775
references: Neuron. 2006 Mar 16;49(6):861-75
references: 16543134
references: Brain Res. 1986 Nov 29;398(2):266-75
references: 3801904
references: Nature. 1978 May 25;273(5660):297-8
references: 418358
references: Neuroscience. 2004;125(3):615-23
references: 15099675
references: Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3525-30
references: 11248111
references: J Neurosci. 2001 Aug 1;21(15):5568-73
references: 11466428
references: Neurobiol Aging. 2012 Feb;33(2):421.e17-28
references: 21030115
references: J Neurosci. 2010 Jun 2;30(22):7507-15
references: 20519525
references: Nature. 2009 Dec 17;462(7275):920-4
references: 19946265
references: J Neurosci. 2006 Mar 15;26(11):3021-9
references: 16540580
references: J Neurosci. 2001 Aug 15;21(16):6245-51
references: 11487647
references: Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3121-5
references: 8610179
references: J Comp Neurol. 1996 Sep 09;373(1):108-17
references: 8876466