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Intraseptal cholinergic infusions alter memory in the rat: method and mechanism

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Neurotransmitter Interactions and Cognitive Function

Part of the book series: Experientia Supplementum ((EXS,volume 98))

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References

  1. Petsch H, Stumpf G, Gogolak C (1962) The significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroenceph Clin Neurophysiol 14: 202–211

    Article  Google Scholar 

  2. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neurosci 81: 893–926

    Article  CAS  Google Scholar 

  3. Toth K, Borhegyi Z, Freund TF (1993) Postsynaptic targets of gabaergic hippocampal neurons in the medial septum-diagonal band of Broca complex. J Neurosci 13: 3712–3724

    PubMed  CAS  Google Scholar 

  4. Gulyas AI, Hajos N, Katona I, Freund TF (2003) Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur J Neurosci 17: 1861–1872

    Article  PubMed  CAS  Google Scholar 

  5. Vertes RP (1981) An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J Neurophysiol 46: 1140–1159

    PubMed  CAS  Google Scholar 

  6. Jakab R, Leranth C (1995) Septum. In: Paxinos G (ed): The rat nervous system. Academic Press, San Diego, 405–442

    Google Scholar 

  7. Gerashchenko D, Salin-Pascual R, Shiromani PJ (2001) Effects of hypocretin-saporin injections into the medial septum on sleep and hippocampal theta. Brain Res 913: 106–115

    Article  PubMed  CAS  Google Scholar 

  8. Coyle JT, Price DL, DeLong MR (1983) Alzheimer’s disease: a disorder of cortical cholinergic innervation. Science 219: 1184–1190

    Article  PubMed  CAS  Google Scholar 

  9. Butcher LL, Woolf NJ (1989) Neurotrophic agents exacerbate the pathologic cascade of Alzheimer’s disease. Neurobiol Aging 10: 557–570

    Article  PubMed  CAS  Google Scholar 

  10. DeKosky ST, Ikonomovic MD, Styren SD, Beckett L, Wisniewski S, Bennett DA, Cochran EJ, Kordower JH, Mufson EJ (2002) Upregulation of choline acetyltransferase activity in hippocampus and from cortex of elderly subjects with mild cognitive impairment. Ann Neurol 51: 145–155

    Article  PubMed  CAS  Google Scholar 

  11. Ikonomovic MD, Mufson EJ, Wuu J, Cochran EJ, Bennett DA, DeKosky ST (2003) Cholinergic plasticity in hippocampus of individuals with mild cognitive impairment: correlation with Alzheimer’s neuropathology. J Alzheimers Dis 5: 39–48

    PubMed  CAS  Google Scholar 

  12. Alreja M, Wu M, Liu, W, Atkins JB, Leranth C, Shanabrough M (2000) Muscarinic tone sustain impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J Neurosci 20: 8103–8110

    PubMed  CAS  Google Scholar 

  13. Barnes CA, Meltzer J, Houston F, Orr G, McGann K, Wenk GL (2000) Chronic treatment of old rats with donepezil or galantamine: effects on memory, hippocampal plasticity and nicotinic receptors. Neuroscience 99: 17–23

    Article  PubMed  CAS  Google Scholar 

  14. Bunce JG, Sabolek HR, Chrobak JJ 2003. Intraseptal infusion of oxotremorine impairs memory in a delayed-non-match-to-sample radial maze task. Neuroscience 121: 259–267

    Article  PubMed  CAS  Google Scholar 

  15. Bunce JG, Sabolek HR, Chrobak JJ (2004) Intraseptal infusion of the cholinergic agonist carbachol impairs delayed-non-match-to-sample radial arm maze performance in the rat. Hippocampus 14: 450–459

    Article  PubMed  Google Scholar 

  16. Bunce JG, Sabolek HR, Chrobak JJ (2004) Timing of administration mediates the memory effects of intraseptal carbachol infusion. Neuoscience 127: 593–600

    Article  CAS  Google Scholar 

  17. Sabolek HR, Bunce JG, Chrobak JJ (2004). Intraseptal tacrine can enhance memory in cognitively impaired young rats. Neuroreport 15: 181–183

    Article  PubMed  Google Scholar 

  18. Sabolek HR, Bunce JG, Giuliana D, Chrobak JJ (2005) Intraseptal tacrine-induced disruptions of spatial memory performance. Behav Brain Research 158: 1–7

    Article  CAS  Google Scholar 

  19. Monmaur P, Breton P (1991) Elicitation of hippocampal theta by intraseptal carbachol injection in freely-moving rats. Brain Research 544: 150–155

    Article  PubMed  CAS  Google Scholar 

  20. Givens BS, Olton DS (1995) Bidirectional modulation of scopolamine-induced working memory impairments by muscarinic activation of the medial septal area. Neurobiol Learning Memory 63: 269–276

    Article  CAS  Google Scholar 

  21. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62: 1033–1047

    Article  PubMed  CAS  Google Scholar 

  22. Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16: 3056–3066

    PubMed  CAS  Google Scholar 

  23. Rye DB, Wainer BH, Mesulam MM, Mufson EJ, Saper CB 1984. Cortical projections arising from the basal forebrain: A study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13: 627–643

    Article  PubMed  CAS  Google Scholar 

  24. Amaral DG, Kurz J, (1985)Ananalysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240: 37–59

    Article  PubMed  CAS  Google Scholar 

  25. Freund T, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336: 170–173

    Article  PubMed  CAS  Google Scholar 

  26. Manns ID, Mainville L, Jones BE (2001) Evidence for glutamate, in addition to acetylcholine and GABA, neurotransmitter synthesis in basal forebrain neurons projecting to the entorhinal cortex. Neuroscience 107: 249–263

    Article  PubMed  CAS  Google Scholar 

  27. Bland BH (1986) Physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26: 1–54

    Article  PubMed  CAS  Google Scholar 

  28. Vinogradova OS (1995) Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45: 523–83

    Article  PubMed  CAS  Google Scholar 

  29. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33: 325–340

    Article  PubMed  CAS  Google Scholar 

  30. Stewart M, Fox SE (1991) Hippocampal theta activity in monkeys. Brain Res 538: 59–63

    Article  PubMed  CAS  Google Scholar 

  31. Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madison JR (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399: 781–784

    Article  PubMed  CAS  Google Scholar 

  32. Amaral DG, Witter M (1995) The three dimension organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571–591

    Article  Google Scholar 

  33. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neurosci 16: 218–222

    Article  PubMed  CAS  Google Scholar 

  34. Hasselmo ME, Schnell E (1994) Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14: 3898–3914

    PubMed  CAS  Google Scholar 

  35. Hasselmo ME, Wyble BP, Wallenstein GV (1996) Encoding and retrieval of episodicmemories: role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6: 693–708

    Article  PubMed  CAS  Google Scholar 

  36. Hasselmo ME (2000) What is the function of the theta rhythm? In: Numan R (ed): The behavioral neuroscience of the septal region, Springer-Verlag, New York, 92–114

    Google Scholar 

  37. Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002) Neuromodulation, theta rhythm and rat spatial navigation. Neural Networks 15: 689–707

    Article  PubMed  Google Scholar 

  38. Chrobak JJ, Lorincz A, Buzsaki G (2000) Physiological patterns in the hippocampoentorhinal cortex system. Hippocampus 10: 457–465

    Article  PubMed  CAS  Google Scholar 

  39. Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201: 160–163

    Article  PubMed  CAS  Google Scholar 

  40. Mitchell SJ, Rawlins JN Steward O, Olton DS (1982) Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J Neurosci 2: 292–302

    PubMed  CAS  Google Scholar 

  41. Givens BS, Olton DS (1990) Cholinergic and GABAergic modulation of medial septal area: effect on working memory. Behav Neurosci 104: 849–855

    Article  PubMed  CAS  Google Scholar 

  42. Markowska A, Olton DS, Givens B (1995) Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology. J Neurosci 15: 2063–2073

    PubMed  CAS  Google Scholar 

  43. Dickson CT, Magistretti J, Shalinsky M, Hamam B, Alonso A (2000) Oscillatory activity in entorhinal neurons and circuits. Mechansisms and function. Ann NY Acad Sci 911: 127–150

    Article  PubMed  CAS  Google Scholar 

  44. Bartus RT, Dean RL 3rd, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408–414

    Article  PubMed  CAS  Google Scholar 

  45. Mesulam MM, Mufson EJ, Wainer BH, Levey AL (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1–Ch6). Neuroscience 10: 1185–1201

    Article  PubMed  CAS  Google Scholar 

  46. Dunnett SB, Fibiger HC (1993) Role of forebrain cholinergic systems in learning and memory: relevance to the cognitive deficits of aging and Alzheimer’s dementia. Prog Brain Res 98: 413–420

    Article  PubMed  CAS  Google Scholar 

  47. Sarter M, Bruno JP (1997) Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Brain Res Rev 23: 28–46

    Article  PubMed  CAS  Google Scholar 

  48. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7: 733–741

    PubMed  CAS  Google Scholar 

  49. Colgin LL, Kramar EA, Gall CM, Lynch G (2003) Septal modulation of excitatory transmission in hippocampus. J Neurophys 90: 2358–2366

    Article  Google Scholar 

  50. Hajos M, Hoffmann WE, Orban G, Kiss T, Erdi P (2004) Modulation of septohippocampal theta activity by GABA-A receptors: an experimental and computational approach. Neuroscience 126: 599–610

    Article  PubMed  CAS  Google Scholar 

  51. Yoder R, Pang KCH (2005) Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 15: 381–392

    Article  PubMed  CAS  Google Scholar 

  52. Rouse ST, Levey AI (1996) Expression of m1–m4 muscarinic acetylcholine receptors immunoreactivity in septohippocampal neurons and other identified hippocampal afferents. J Comp Neurol 375: 406–416

    Article  PubMed  CAS  Google Scholar 

  53. Lawson VH, Bland BH (1993) The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine and procaine. Exp Neurol 120: 132–144

    Article  PubMed  CAS  Google Scholar 

  54. Birthelmer A, Lazaris A, Riegert C, Marques Pereira P, Koenig J, Jeltsch H, Jackisch R, Cassel JC (2003) Does the release of acetylcholine in septal slices originate from intrinsic cholinergic neurons bearing p75(NTR) receptors? A study using 192 IgG-saporin lesions in rats. Neuroscience 122: 1059–1071

    Article  PubMed  CAS  Google Scholar 

  55. Luttgen M, Ogren SO, Meister B (2005) 5-HT1A receptor mRNA and immunoreactivity in the rat medial septum/diagonal band of broca-relationships to GABAergic and cholinergic neurons. J Chem Neuroanat 29: 93–111

    Article  PubMed  CAS  Google Scholar 

  56. Kosis B, Li S (2004) In vivo contribution of h-channels in the septal pacemaker to theta rhythm generation. Eur J Neurosci 20: 1249–2158

    Google Scholar 

  57. Nader K (2003) Memory traces unbound. Trends Neurosci 26: 65–72

    Article  PubMed  CAS  Google Scholar 

  58. Lee I, Kesner RP (2003) Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23: 1517–1523

    PubMed  CAS  Google Scholar 

  59. Frick KM, Gorman LK, Markowska AL (1996) Oxotremorine infusions into the medial septum of middle-aged rats affect spatial reference memory and ChAT activity. Behav Brain Res 80: 99–109

    Article  PubMed  CAS  Google Scholar 

  60. Flood JF, Farr SA, Uezu K, Morley JE (1998) The pharmacology of post-trial memory processing in septum. Eur J Pharmacol 350: 31–38

    Article  PubMed  CAS  Google Scholar 

  61. Pang KC, Nocera R (1999). Interactions between 192-IgG saporine and intraseptal cholinergic and GABAergic drugs: role of cholinergic medial septal neurons in spatial working memory. Behav Neurosci 113: 265–275

    Article  PubMed  CAS  Google Scholar 

  62. Farr SA, Flood JF, Morley JE (2000) The effect of cholinergic, GABAergic, serotonergic, and glutamatergic receptor modulation on posttrial memory processing in the hippocampus. Neurobiol Learn Mem 73: 150–167

    Article  PubMed  CAS  Google Scholar 

  63. Hagan JJ, Salamone JD, Simpson J, Iversen SD, Morris RGM (1988) Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis. Behav Brain Res 27: 9–20

    Article  PubMed  CAS  Google Scholar 

  64. Wenk GL Harrington CA, Tucker DA, Rance NE, Walker LC (1992) Basal forebrain lesions and memory: a biochemical, histological and behavioral study of differential vulnerability to ibotenate and quisqualate. Behav Neurosci 106: 909–923

    Article  PubMed  CAS  Google Scholar 

  65. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995) Selective immunotoxic lesions of basal forebrain cholinergic cells:effects on learning and memory in rats. Behav Neurosci 4: 714–722

    Article  Google Scholar 

  66. Shen J, Barnes CA, Wenk GL, McNaughton B (1996) Differential effects of selective immunotoxic lesions of medial septal cholinergic cells on spatial working and reference memory. Behav Neurosci 110: 1181–1186

    Article  PubMed  CAS  Google Scholar 

  67. Walsh Tj Herzon CD, Gandhi C, Stackman RW, Wiley RG (1996) Injection IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res 726: 69–78

    Article  PubMed  CAS  Google Scholar 

  68. McMahon RW, Sobel TJ, Baxter MG (1997) Selective immunolesions of hippocampal cholinergic inpu fail to impair spatial working memory. Hippocampus 7: 130–136

    Article  Google Scholar 

  69. Chang O, Gold PE (2004) Impaired and spared cholinergic functions in the hippocampus after lesions of the medial septum/vertical limb of the diagonal band with 192 IgG saporin. Hippocampus 14: 170–179

    Article  PubMed  CAS  Google Scholar 

  70. Mulder J, Harkany T, Czollner K, Cremers TI, Keijser JN, Nyakas C, Luiten PG (2005) Galantamine-induced behavioral recovery after sublethal excitotoxic lesions of medial septum. Behav Brain Res 67: 117–125

    Google Scholar 

  71. Wallenstein GV, Hasselmo ME (1997) Functional transitions between epileptiform-like activity and associative memory in hippocampal region CA3. Brain Res Bull 43: 485–93

    Article  PubMed  CAS  Google Scholar 

  72. Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21: 317–323

    Article  PubMed  CAS  Google Scholar 

  73. Gauthier SG (2005) Alzheimer’s disease: the benefits of early treatment. E J Neurol 12: 11–16

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology, University of Connecticut, Storrs, CT, 06269, USA

    James J. Chrobak, Helen R. Sabolek & Jamie G. Bunce

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  1. James J. Chrobak
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  2. Helen R. Sabolek
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  3. Jamie G. Bunce
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  1. Department of Psychiatry and Behavioral Sciences Neurobehavioural Research Laboratory, Duke University Medical Center, Box 3412, Durham, NC, 27710, USA

    Edward D. Levin

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Chrobak, J.J., Sabolek, H.R., Bunce, J.G. (2006). Intraseptal cholinergic infusions alter memory in the rat: method and mechanism. In: Levin, E.D. (eds) Neurotransmitter Interactions and Cognitive Function. Experientia Supplementum, vol 98. Birkhäuser Basel. https://doi.org/10.1007/978-3-7643-7772-4_5

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