Sex differences in the septo-hippocampal cholinergic system in rats: Behavioral consequences

Current Topics in Behavioral Neurosciences

Volumn 8, Issue , 2011, Pages 57-71

  Mitsushima, Dai ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Acetylcholine; Androgen; Diurnal rhythm; Estrogen; Learning and memory; Sex difference

Indexed keywords

ACETYLCHOLINE; ANDROGEN; DONEPEZIL; ESTRADIOL; MUSCIMOL; NALOXONE; TESTOSTERONE; CHOLINERGIC RECEPTOR STIMULATING AGENT; STEROID;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ARTICLE; CHOLINERGIC SYSTEM; DOWN REGULATION; HIPPOCAMPAL CA1 REGION; HORMONAL REGULATION; HUMAN; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROMODULATION; NEUROMONITORING; NEUROPATHOLOGY; NEUROPHYSIOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; SPATIAL MEMORY; UPREGULATION; ANIMAL; CASTRATION; DRUG EFFECT; FEMALE; HIPPOCAMPUS; MALE; METABOLISM; METHODOLOGY; RAT; REVIEW; SEPTUM PELLUCIDUM; SEXUAL DEVELOPMENT; TIME;

ACETYLCHOLINE; ANIMALS; CASTRATION; CHOLINERGIC AGENTS; FEMALE; HIPPOCAMPUS; MALE; RATS; SEPTUM OF BRAIN; SEX CHARACTERISTICS; STEROIDS; TIME FACTORS;

EID: 80053328124     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2010_95     Document Type: Article

References (87)

1. Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492:479-493
2. BeattyWW(1984) Hormonal organization of sex differences in play fighting and spatial behavior. Prog Brain Res 61:315-330
3. Brown RT (1968) Early experience and problem-solving ability. J Comp Physiol Psychol 65:433-440
4. Buzsáki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 8:4007-4026
5. Cherrier MM, Matsumoto AM, Amory JK, Asthana S, Bremner W, Peskind ER, Raskind MA, Craft S (2005) Testosterone improves spatial memory in men with Alzheimer disease and mild cognitive impairment. Neurology 64:2063-2068
6. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299-1301
7. Coyle JT, Price DL, DeLong MR (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219:1184-1190
8. Cummings JL (2004) Alzheimer's disease. N Engl J Med 351:56-67
9. Daniel JM, Fader AJ, Spencer AL, Dohanich GP (1997) Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225
10. Day J, Damsma G, Fibiger HC (1991) Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav 38:723-729
11. Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GC, Scheiner ZS, Storm DR (2008) Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat Neurosci 11:1074-1082
12. Einon D (1980) Spatial memory and response strategies in rats: age, sex and rearing differences in performance. Q J Exp Psychol 32:473-489
13. Endo Y, Mizuno T, Fujita K, Funabashi T, Kimura F (1994) Soft-diet feeding during development enhances later learning abilities in female rats. Physiol Behav 56:629-633
14. Falvo RE, Buhl A, Nalbandov AV (1974) Testosterone concentrations in the peripheral plasma of androgenized female rats and in the estrous cycle of normal female rats. Endocrinology 95:26-29
15. Fernández de Sevilla D, Núñez A, Borde M, Malinow R, Buño W (2008) Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J Neurosci 28:1469-1478
16. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Hasegawa K, Hendrie H, Huang Y, Jorm A, Mathers C, Menezes PR, Rimmer E, Scazufca M (2005) Global prevalence of dementia: a Delphi consensus study. Lancet 366:2112-2117
17. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322:96-101
18. Gibbs RB, Pfaff DW (1992) Effects of estrogen and fimbria/fornix transaction on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116:23-39
19. Gold PE (2003) Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem 80:194-210
20. Greenough WT, Madden TC, Fleischmann TB (1972) Effects of isolation, daily handling, and enriched rearing on maze learning. Psychon Sci 27:279-280
21. Herrera-Morales W, Mar I, Serrano B, Bermúdez-Rattoni F (2007) Activation of hippocampal postsynaptic muscarinic receptors is involved in long-term spatial memory formation. Eur J Neurosci 25:1581-1588
22. Hironaka N, Tanaka K, Izaki Y, Hori K, Nomura M (2001) Memory-related acetylcholine efflux from the rat prefrontal cortex and hippocampus: a microdialysis study. Brain Res 901:143-150
23. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731
24. Hymovitch B (1952) The effects of experimental variations on problem solving in the rat. J Comp Physiol Psychol 45:313-321
25. Juraska JM, Henderson C, Muller J (1984) Differential rearing experience, gender, and radial maze performance. Dev Psychobiol 17:209-215
26. Komorowski RW, Manns JR, Eichenbaum H (2009) Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J Neurosci 29:9918-9929
27. Kotani S, Yamauchi T, Teramoto T, Ogura H (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142:505-514
28. Kritzer MF (1997) Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat. J Comp Neurol 379:247-260
29. Kritzer MF, McLaughlin PJ, Smirlis T, Robinson JK (2001) Gonadectomy impairs T-maze acquisition in adult male rats. Horm Behav 39:167-174
30. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsáki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047
31. Luine VN, Renner KJ, McEwen BS (1986) Sex-dependent differences in estrogen regulation of choline acetyltransferase are altered by neonatal treatments. Endocrinology 119:874-878
32. Luine V, Jacome LF, MacLusky NJ (2003) Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144:2836-2844
33. Lund TD, Hinds LR, Handa RJ (2006) The androgen 5a-dihydrotestosterone and its metabolite 5a-androstan-3b, 17b-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor b-expressing neurons in the hypothalamus. J Neurosci 26:1448-1456
34. Markowska AJ, Savonenko AV (2002) Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci 22: 10985-10995
35. Markram H, Segal M (1990) Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol 427:381-393
36. Masuda J, Mitsushima D, Funabashi T, Kimura F (2005) Sex and housing conditions affect the 24-h acetylcholine release profile in the hippocampus in rats. Neuroscience 132:537-542
37. McCurry SM, Logsdon RG, Vitiello MV, Teri L (2004) Treatment of sleep and nighttime disturbances in Alzheimer's disease: a behavior management approach. Sleep Med 5:373-377
38. McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303-1311
39. McEwen BS, Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20:279-307
40. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201
41. Miettinen RA, Kalesnykas G, Koivisto EH (2002) Estimation of the total number of cholinergic neurons containing estrogen receptor-a in the rat basal forebrain. J Histochem Cytochem 50:891-902
42. Mitsushima D, Mizuno T, Kimura F (1996) Age-related changes in diurnal acetylcholine release in the prefrontal cortex of male rats as measured by microdialysis. Neuroscience 72:429-434
43. Mitsushima D, Yamanoi C, Kimura F (1998) Restriction of environmental space attenuates locomotor activity and hippocampal acetylcholine release in male rats. Brain Res 805:207-212
44. Mitsushima D, Funabashi T, Shinohara K, Kimura F (2001) Impairment of maze learning in rats by restricting environmental space. Neurosci Lett 297:73-76
45. Mitsushima D, Masuda J, Kimura F (2003a) Sex differences in the stress-induced release of acetylcholine in the hippocampus and corticosterone from the adrenal cortex in rats. Neuroendocrinology 78:234-240
46. Mitsushima D, Tin-Tin-Win-Shwe, Kimura F (2003b) Sexual dimorphism in the GABAergic control of gonadotropin release in intact rats. Neurosci Res 46:399-405
47. Mitsushima D, Takase K, Funabashi T, Kimura F (2008) Gonadal steroid hormones maintain the stress-induced acetylcholine release in the hippocampus: simultaneous measurements of the extracellular acetylcholine and serum corticosterone levels in the same subjects. Endocrinology 149:802-811
48. Mitsushima D, Takase K, Funabashi T, Kimura F (2009) Gonadal steroids maintain 24-h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J Neurosci 29:3808-3815
49. Mizuno T, Kimura F (1996) Medial septal injection of naloxone elevates acetylcholine release in the hippocampus and induces behavioral seizures in rats. Brain Res 713:1-7
50. Mizuno T, Endo Y, Arita J, Kimura F (1991) Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience 44:607-612
51. Moffat SD, Zonderman AB, Metter EJ, Kawas C, Blackman MR, Harman SM, Resnick SM (2004) Free testosterone and risk for Alzheimer disease in older men. Neurology 62:188-193
52. Mohapel P, Leanza G, Kokaia M, Lindvall O (2005) Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 26:939-946
53. Moor E, DeBoer P, Westerink BHC (1998) GABA receptors and benzodiazepine binding sites modulate hippocampal acetylcholine release in vivo. Eur J Pharmacol 359:119-126
54. Mount C, Downtown D (2006) Alzheimer disease: progress or profit? Nat Med 12:780-784
55. Mufson EJ, Cai WJ, Jaffar S, Chen E, Stebbins G, Sendera T, Kordower JH (1999) Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res 849:253-274
56. Nakamura N, Fujita H, KawataM(2002) Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 109:473-485
57. Nilsson OG, Leanza G, Bjorklund A (1992) Acetylcholine release in the hippocampus: regulation by monoaminergic afferents as assessed by in vivo microdialysis. Brain Res 584:132-140
58. Norbury R, Travis MJ, Erlandsson K, Waddington W, Ell PJ, Murphy DGM (2007) Estrogen therapy and brain muscarinic receptor density in healthy females: a SPET study. Horm Behav 51:249-257
59. Parducz A, Hajszan T, Maclusky NJ, Hoyk Z, Csakvari E, Kurunczi A, Prange-Kiel J, Leranth C (2006) Synaptic remodeling induced by gonadal hormones: neuronal plasticity as a mediator of neuroendocrine and behavioral responses to steroids. Neuroscience 138:977-985
60. Parent MB, Baxter MG (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem 11:9-20
61. Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trend Neurosci 22:273-280
62. Petersen RC, Thomas RG, Grundman M, Bennett D, Doody R, Ferris S, Galasko D, Jin S, Kaye J, Levey A, Pfeiffer E, Sano M, van Dyck CH, Thal LJ (2005) Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med 352:2379-2388
63. Pongrac JL, Gibbs RB, Defranco DB (2004) Estrogen-mediated regulation of cholinergic expression in basal forebrain neurons requires extracellular signal-regulated kinase activity. Neuroscience 124:809-816
64. Ragozzino ME, Unick KE, Gold PE (1996) Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc Natl Acad Sci USA 93:4693-4698
65. Romeo RD, McCarthy JB, Wang A, Milner TA, McEwen BS (2005) Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-a. Neuroendocrinology 81:391-399
66. Rosario ER, Chang L, Stanczyk FZ, Pike CJ (2004) Age-related testosterone deplation and the development of Alzheimer disease. JAMA 292:1431-1432
67. Rush ME, Blake CA (1982) Serum testosterone concentrations during the 4-day estrous cycle in normal and adrenalectomized rats. Proc Soc Exp Biol Med 169:216-221
68. Sarter M, Parikh V (2005) Choline transporters, cholinergic transmission and cognition. Nat Neurosci 6:48-56
69. 2 muscarinic acetylcholine receptor knock-out mice show deficits in behavioral flexibility, working memory, and hippocampal plasticity. J Neurosci 24: 10117-10127
70. Seymoure P, Dou H, Juraska JM (1996) Sex differences in radial maze performance: influence of rearing environment and room cues. Psychobiology 24:33-37
71. 1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25:11194-11200
72. Shors TJ, Chua C, Falduto J (2001) Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292-6297
73. Smith HV (1972) Effects of environmental enrichment on open-field activity and Hebb-Williams problem solving in rats. J Comp Physiol Psychol 80:163-168
74. Stancampiano R, Cocco S, Cugusi C, Sarais L, Fadda F (1999) Serotonin and acetylcholine release response in the rat hippocampus during a spatial memory task. Neuroscience 89:1135-1143
75. Starkstein SE, Jorge R, Mizrahi R, Robinson RG (2005) The construct of minor and major depression in Alzheimer's disease. Am J Psychiatry 162:2086-2093
76. Swaab DF, Hofman MA (1995) Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation. Trend Neurosci 18:264-270
77. Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321-353
78. Takase K, Funabashi T, Mogi K, Mitsushima D, Kimura F (2005a) Feeding with powdered diet after weaning increases visuospatial ability in association with increases in the expression of N-methyl-D-aspartate receptors in the hippocampus of female rats. Neurosci Res 53:169-175
79. Takase K, Mitsushima D, Masuda J, Mogi K, Funabashi T, Endo Y, Kimura F (2005b) Feeding with powdered diet after weaning affects sex difference in acetylcholine release in the hippocampus in rats. Neuroscience 136:593-599
80. Takase K, Kimura F, Yagami T, Mitsushima D (2009) Sex-specific 24-h acetylcholine release profile in the medial prefrontal cortex: simultaneous measurement of spontaneous locomotor activity in behaving rats. Neuroscience 159:7-15
81. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431
82. 2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA 88:1859-1863
83. Widmer H, Ferrigan L, Davies CH, Cobb SR (2006) Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 16:617-628
84. Williams CL, Meck WH (1991) The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16:155-176
85. Winblad B, Kilander L, Eriksson S, Minthon L, Batsman S, Wetterholm AL, Jansson-Blixt C, Haglund A (2006) Donepezil in patients with severe Alzheimer's disease: double-blind, parallel-group, placebo-controlled study. Lancet 367:1057-1065
86. Yanai J, Rogel-Fuchs Y, Pick CG, Slotkin T, Seidler FJ, Zahalka EA, Newman ME (1993) Septohippocampal cholinergic changes after destruction of the A10-septal dopaminergic pathways. Neuropharmacology 32:113-117
87. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC, Breitner JCS (2002) Hormone replacement therapy and incidence of Alzheimer disease in older women. JAMA 288:2123-2129