Basal Forebrain Cholinergic System and Memory

Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 37)

Abstract

Basal forebrain cholinergic neurons constitute a way station for many ascending and descending pathways. These cholinergic neurons have a role in eliciting cortical activation and arousal. It is well established that they are mainly involved in cognitive processes requiring increased levels of arousal, attentive states and/or cortical activation with desynchronized activity in the EEG. These cholinergic neurons are modulated by several afferents of different neurotransmitter systems. Of particular importance within the cortical targets of basal forebrain neurons is the hippocampal cortex. The septohippocampal pathway is a bidirectional pathway constituting the main septal efferent system, which is widely known to be implicated in every memory process investigated. The present work aims to review the main neurotransmitter systems involved in modulating cognitive processes related to learning and memory through modulation of basal forebrain neurons.

Keywords

Acetylcholine Learning Modulation Consolidation GABA Glutamate Noradrenaline Hypocretin Orexin Vasopressin Oxytocin Substance P 

References

  1. Albuquerque EX, Pereira EFR, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73–120PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bartfai T, Bedecs K, Land T, Langel U, Bertorelli R, Girotti P, Consolo S, Xu XJ, Wiesenfeld-Hallin Z, Nilsson S et al (1991) M-15: high-affinity chimeric peptide that blocks the neuronal actions of galanin in the hippocampus, locus coeruleus, and spinal cord. Proc Natl Acad Sci USA 88(23):10961–5PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Sci 217:408–414CrossRefGoogle Scholar
  4. Basheer R, Bauer A, Elmenhorst D, Ramesh V, McCarley RW (2007) Sleep deprivation upregulates A1 adenosine receptors in the rat basal forebrain. NeuroReport 18:1895–1899PubMedCrossRefGoogle Scholar
  5. Basheer R, Halldner L, Alanko L, McCarley RW, Fredholm BB, Porkka-Heiskanen T (2001) Opposite changes in adenosine A1 and A2A receptor mRNA in the rat following sleep deprivation. Neuroreport 12(8):1577–1580PubMedCrossRefGoogle Scholar
  6. Beal MF, MacGarvey U, Swartz KJ (1990) Galanin immunoreactivity is increased in the nucleus basalis of Meynert in Alzheimer’s disease. Ann Neurol 28(2):157–161PubMedCrossRefGoogle Scholar
  7. Belarbi K, Schindowski K, Burnouf S, Caillierez R, Grosjean ME, Demeyer D, Hamdane M, Sergeant N, Blum D, Buée L (2009) Early Tau pathology involving the septo-hippocampal pathway in a Tau transgenic model: relevance to Alzheimer’s disease. Curr Alzheimer Res 6(2):152–157PubMedPubMedCentralCrossRefGoogle Scholar
  8. Benzing WC, Kordower JH, Mufson EJ (1993) Galanin immunoreactivity within the primate basal forebrain: evolutionary change between monkeys and apes. J Comp Neurol 336(1):31–39PubMedCrossRefGoogle Scholar
  9. Bertorelli R, Forloni G, Consolo S (1991) Modulation of cortical in vivo acetylcholine release by the basal nuclear complex: role of the pontomesencephalic tegmental area. Brain Res 563:353–356PubMedCrossRefGoogle Scholar
  10. Bierer LM, Haroutunian V, Gabriel S, Knott PJ, Carlin LS, Purohit DP, Perl DP, Schmeidler J, Kanof P, Davis KL (1995) Neurochemical correlates of dementia severity in Alzheimer’s disease: relative importance of the cholinergic deficits. J Neurochem 64(2):749–760PubMedCrossRefGoogle Scholar
  11. Blokland A (1995) Acetylcholine: a neurotransmitter for learning and memory? Brain Res Rev 21:285–300PubMedCrossRefGoogle Scholar
  12. Boccia MM, Baratti CM (2000) Involvement of central cholinergic mechanisms in the effects of oxytocin and an oxytocin receptor antagonist on retention performance in mice. Neurobiol Learn Mem 74(3):217–228PubMedCrossRefGoogle Scholar
  13. Boccia MM, Kopf SR, Baratti CM (1998) Effects of a single administration of oxytocin or vasopressin and their interactions with two selective receptor antagonists on memory storage in mice. Neurobiol Learn Mem 69(2):136–146PubMedCrossRefGoogle Scholar
  14. Bondareff W, Mountjoy CQ, Roth M, Rossor MN, Iversen LL, Reynolds GP, Hauser DL (1987) Neuronal degeneration in locus ceruleus and cortical correlates of Alzheimer disease. Alzheimer Dis Assoc Disord 1:256–262PubMedCrossRefGoogle Scholar
  15. Bubser M, Byun N, Wood MR, Jones CK (2012) Muscarinic receptor pharmacology and circuitry for the modulation of cognition. Handb Exp Pharmacol 208:121–166CrossRefGoogle Scholar
  16. Chang HC, Gaddum JH (1933) Choline esters in tissue extracts. J Physiol 79:255–285PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chan‐Palay V (1988) Galanin hyperinnervates surviving neurons of the human basal nucleus of Meynert in dementias of Alzheimer’s and Parkinson’s disease: a hypothesis for the role of galanin in accentuating cholinergic dysfunction in dementia. J Comp Neurol 273(4): 543–557PubMedCrossRefGoogle Scholar
  18. Chan-Palay V (1991) Alterations in the locus coeruleus in dementias of Alzheimer’s and Parkinson’s disease. Prog Brain Res 88:625–630PubMedCrossRefGoogle Scholar
  19. Chen HS, Lipton SA (2006) The chemical biology of clinically tolerated NMDA receptor antagonist. J Neurochem 97:1611–1626PubMedCrossRefGoogle Scholar
  20. Cornwell-Jones CA, Decker MW, Chang JW, Cole B, Goltz KM, Tran T et al (1989) Neonatal 6-hydroxydopa, but not DSP-4, elevates brainstem monoamines and impairs inhibitory avoidance learning in developing rats. Brain Res 493:258–268PubMedCrossRefGoogle Scholar
  21. Counts SE, Perez SE, Ginsberg SD, Mufson EJ (2010) Neuroprotective role for galanin in Alzheimer’s disease. Experientia Suppl 102:143–162CrossRefGoogle Scholar
  22. Court J, Martin-Ruiz C, Piggott M, Spurden D, Griffiths M, Perry E (2001) Nicotinic receptor abnormalities in Alzheimer’s disease. Biol Psychiatry 49(3):175–184PubMedCrossRefGoogle Scholar
  23. Coyle JT, Price DL, DeLong MR (1983) Alzheimer’s disease: a disorder of cortical cholinergic innervation. Sci 219(4589):1184–1190CrossRefGoogle Scholar
  24. Crawley JN (1996) Galanin-acetylcholine interactions: relevance to memory and Alzheimer’s disease. Life Sci 58(24):2185–2199PubMedCrossRefGoogle Scholar
  25. Crawley JN, Mufson EJ, Hohmann JG, Teklemichael D, Steiner RA, Holmberg K, Xu ZQ, Blakeman KH, Xu XJ, Wiesenfeld-Hallin Z, Bartfai T, Hökfelt T (2002) Galanin overexpressing transgenic mice. Neuropeptides 36(2–3):145–156PubMedCrossRefGoogle Scholar
  26. Dale HH, Dudley HW (1929) The presence of histamine and acetylcholine in the spleen of the ox and the horse. J Physiol (Lond) 68:97–123CrossRefGoogle Scholar
  27. Dale HH, Laidlaw PP, Symons CT (1910) A reversed action of the vagus on the mammalian heart. J Physiol (Lond) 41:1–18CrossRefGoogle Scholar
  28. Dalrymple-Alford JC (1994) Behavioral effects of basal forebrain grafts after dorsal septohippocampal pathway lesions. Brain Res 661(1–2):243–258PubMedCrossRefGoogle Scholar
  29. Dannenberg H, Pabst M, Braganza O, Schoch S, Niediek J, Bayraktar M, Mormann F, Beck H (2015) Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks. J Neuroscience 35(22):8394–8410CrossRefGoogle Scholar
  30. Decker MW, McGaugh JL (1991) The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 7(2):151–168PubMedCrossRefGoogle Scholar
  31. Di Cesare Mannelli L, Tenci B, Zanardelli M et al (2015) α7 Nicotinic Receptor Promotes the Neuroprotective Functions of Astrocytes against Oxaliplatin Neurotoxicity. Neural Plast 2015:396908Google Scholar
  32. Díaz-Cabiale Z, Flores-Burgess A, Parrado C, Narváez M, Millón C, Puigcerver A, Coveñas R, Fuxe K, Narváez JA (2014) Galanin receptor/neuropeptide y receptor interactions in the central nervous system. Curr Protein Pept Sci 15(7):666–672PubMedCrossRefGoogle Scholar
  33. Ding X, MacTavish D, Kar S, Jhamandas JH (2006) Galanin attenuates beta-amyloid (Abeta) toxicity in rat cholinergic basal forebrain neurons. Neurobiol Dis 21(2):413–420PubMedCrossRefGoogle Scholar
  34. dos Santos VV, Santos DB, Lach G, Rodrigues AL, Farina M, De Lima TC, Prediger RD (2013) Neuropeptide Y (NPY) prevents depressive-like behavior, spatial memory deficits and oxidative stress following amyloid-β (Aβ(1–40)) administration in mice. Behav Brain Res 244:107–115PubMedCrossRefGoogle Scholar
  35. Dougherty KD, Milner TA (1999) Cholinergic septal afferent terminals preferentially contact neuropeptide Y-containing interneurons compared to parvalbumin-containing interneurons in the rat dentate gyrus. J Neuroscience 19(22):10140–10152Google Scholar
  36. Dringenberg HC, Olmstead MC (2003) Integrated contributions of basal forebrain and thalamus to neocortical activation elicited by pedunculopontine tegmental stimulation in urethane-anesthetized rats. Neuroscience 119(3):839–853PubMedCrossRefGoogle Scholar
  37. Dutar P, Lamour Y, Nicoll RA (1989) Galanin blocks the slow cholinergic EPSP in CA1 pyramidal neurons from ventral hippocampus. Eur J Pharmacol 164(2):355–360PubMedCrossRefGoogle Scholar
  38. Easton A, Douchamps V, Eacott M, Lever C (2012) A specific role for septohippocampal acetylcholine in memory? Neuropsychologia 50:3156–3168PubMedPubMedCentralCrossRefGoogle Scholar
  39. Eaton K, Sallee FR, Sah R (2007) Relevance of neuropeptide Y (NPY) in psychiatry. Curr Top Med Chem 7(17):1645–1659PubMedCrossRefGoogle Scholar
  40. Eckenstein FP, Baughman RW, Quinn J (1988) An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25:457–474PubMedCrossRefGoogle Scholar
  41. Elliott-Hunt CR, Marsh B, Bacon A, Pope R, Vanderplank P, Wynick D (2004) Galanin acts as a neuroprotective factor to the hippocampus. Proc Natl Acad Sci USA 101(14):5105–5110PubMedPubMedCentralCrossRefGoogle Scholar
  42. Elmslie KS, Yoshikami D (1985) Effects of kynurenate on root potentials evoked by synaptic activity and amino acids in the frog spinal cord. Brain Res 330(2):265–272PubMedCrossRefGoogle Scholar
  43. España RA, Berridge CW (2006) Organization of noradrenergic efferents to arousal-related basal forebrain structures. J Comp Neurol 496(5):668–683PubMedCrossRefGoogle Scholar
  44. Everitt BJ, Robbins TW (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48:649–684PubMedCrossRefGoogle Scholar
  45. Fadel J, Burk JA (2010) Orexin/hypocretin modulation of the basal forebrain cholinergic system: Role in attention. Brain Res 1314:112–123PubMedCrossRefGoogle Scholar
  46. Fadel J, Frederick-Duus D (2008) Orexin/hypocretin modulation of the basal forebrain cholinergic system: insights from in vivo microdialysis studies. Pharmacol Biochem Behav 90(2):156–162PubMedCrossRefGoogle Scholar
  47. Fadel J, Moore H, Sarter M, Bruno JP (1996) Trans-synaptic stimulation of cortical acetylcholine release after partial 192 IgG-saporin-induced loss of cortical cholinergic afferents. J Neuroscience 16:6592–6600Google Scholar
  48. Fadel J, Sarter M, Bruno JP (2001) Basal forebrain glutamatergic modulation of cortical acetylcholine release. Synapse 39:201–212PubMedCrossRefGoogle Scholar
  49. Farr SA, Uezu K, Flood JF, Morley JE (1999) Septo-hippocampal drug interactions in post-trial memory processing. Brain Res 847(2):221–230PubMedCrossRefGoogle Scholar
  50. Fisone G, Wu CF, Consolo S, Nordström O, Brynne N, Bartfai T, Melander T, Hökfelt T (1987) Galanin inhibits acetylcholine release in the ventral hippocampus of the rat: histochemical, autoradiographic, in vivo, and in vitro studies. Proc Natl Acad Sci USA 84(20):7339–7343PubMedPubMedCentralCrossRefGoogle Scholar
  51. Flood JF, Baker ML, Hernandez EN, Morley JE (1989) Modulation of memory processing by neuropeptide Y varies with brain injection site. Brain Res 503(1):73–82PubMedCrossRefGoogle Scholar
  52. Flood JF, Baker ML, Hernandez EN, Morley JE (1990) Modulation of memory retention by neuropeptide K. Brain Res 520(1–2):284–290PubMedCrossRefGoogle Scholar
  53. Flood JF, Hernandez EN, Morley JE (1987) Modulation of memory processing by neuropeptide Y. Brain Res 421(1–2):280–290PubMedCrossRefGoogle Scholar
  54. Flood JF, Morley JE (1989) Dissociation of the effects of neuropeptide Y on feeding and memory: evidence for pre- and postsynaptic mediation. Peptides 10(5):963–966PubMedCrossRefGoogle Scholar
  55. Fort P, Khateb A, Pegna A, Muhlethaler M, Jones BE (1995) Noradrenergic modulation of cholinergic nucleus basalis neurons demonstrated by in vitro pharmacological and immunohistochemical evidence in the guinea-pig brain. Eur J Neuroscience 7:1502–1511CrossRefGoogle Scholar
  56. Francis PT, Palmer AM, Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer’s disease: A review of progress. J Neurol Neurosurg Psychiatry 66(2):137–147PubMedPubMedCentralCrossRefGoogle Scholar
  57. Fritschy JM, Grzanna R (1989) Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 30:181–197PubMedCrossRefGoogle Scholar
  58. Fühner H (1918) Untersuchunge über den Synergismus von Giften. Arch f Exper Pathol u Pharmacol 82:51–80CrossRefGoogle Scholar
  59. Galey D, Toumane A, Durkin T, Jaffard R (1989) In vivo modulation of septo-hippocampal cholinergic activity in mice: relationships with spatial reference and working memory performance. Behav Brain Res 32(2):163–172PubMedCrossRefGoogle Scholar
  60. German DC, Manaye KF, White CL III, Woodward DJ, McIntire DD, Smith WK, Kalaria RN, Mann DM (1992) Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 32:667–676PubMedCrossRefGoogle Scholar
  61. Givens BS, Olton DS, Crawley JN (1992) Galanin in the medial septal area impairs working memory. Brain Res 582(1):71–77PubMedCrossRefGoogle Scholar
  62. Gold PE (2003) Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem 80:194–210PubMedCrossRefGoogle Scholar
  63. Goldbach R, Allgaier C, Heimrich B, Jackisch R (1998) Postnatal development of muscarinic autoreceptors modulating acetylcholine release in the septohippocampal cholinergic system. I. Axon terminal region: hippocampus. Brain Res Dev Brain Res 108(1–2):23–30PubMedCrossRefGoogle Scholar
  64. Gu Z, Cheng J, Zhong P, Qin L, Liu W, Yan Z (2014) Aβ selectively impairs mGluR7 modulation of NMDA signaling in basal forebrain cholinergic neurons: implication in Alzheimer’s disease. J Neuroscience 34(41):13614–13628CrossRefGoogle Scholar
  65. Hammar CG, Hanin I, Holmstedt B et al (1968) Identification of acetylcholine in fresh rat brain by combined gas chromatography-mass spectrometry. Nature 220:915–917PubMedCrossRefGoogle Scholar
  66. Harkany T, Abrahám I, Timmerman W, Laskay G, Tóth B, Sasvári M et al (2000) Beta-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur J Neuroscience 12:2735–2745CrossRefGoogle Scholar
  67. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16:710–715PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hasselmo ME, Sarter M (2011) Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36:52–73PubMedCrossRefGoogle Scholar
  69. Heneka MT, Ramanathan M, Jacobs AH, Dumitrescu-Ozimek L, Bilkei-Gorzo A, Debeir T, Sastre M, Galldiks N, Zimmer A, Hoehn M, Heiss WD, Klockgether T, Staufenbiel M (2006) Locus ceruleus degeneration promotes Alzheimer pathogenesis in amyloid precursor protein transgenic mice. J Neuroscience 26(5):1343–1354CrossRefGoogle Scholar
  70. Hökfelt T, Millhorn D, Seroogy K, Tsuruo Y, Ceccatelli S, Lindh B, Meister B, Melander T, Schalling M, Bartfai T et al (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43(7):768–780PubMedCrossRefGoogle Scholar
  71. Hunt R, Taveau R de M (1906) On the physiological action of cetain cholin derivatives and new methods for detecting cholin. Br Med J 3:1788–1791Google Scholar
  72. Huston JP, Hasenöhrl RU (1995) The role of neuropeptides in learning: focus on the neurokinin substance P. Behav Brain Res 66:117–127PubMedCrossRefGoogle Scholar
  73. Jones BE, Cuello AC (1989) Afferents to the basal forebrain cholinergic cell area from pontomesencephalic–catecholamine, serotonin, and acetylcholine–neurons. Neuroscience 31:37–61PubMedCrossRefGoogle Scholar
  74. Kalinchuk AV, McCarley RW, Porkka-Heiskanen T, Basheer R (2011) The time course of adenosine, nitric oxide (NO) and inducible NO synthase changes in the brain with sleep loss and their role in the non-rapid eye movement sleep homeostatic cascade. J Neurochem 116:260–272PubMedCrossRefGoogle Scholar
  75. Khateb A, Fort P, Williams S, Serafin M, Muhlethaler M, Jones BE (1998) GABAergic input to cholinergic nucleus basalis neurons. Neuroscience 86:937–947PubMedCrossRefGoogle Scholar
  76. Knox D, Sarter M, Berntson GG (2004) Visceral afferent bias on cortical processing: role of adrenergic afferents to the basal forebrain cholinergic system. Behav Neuroscience 118:1455–1459CrossRefGoogle Scholar
  77. Krebs JR (1990) Food-storing birds: adaptive specialization in brain and behaviour? Philos Trans R Soc Lond B Biol Sci 329(1253):153–160PubMedCrossRefGoogle Scholar
  78. Krügel U, Bigl V, Eschrich K, Bigl M (2001) Deafferentation of the septo-hippocampal pathway in rats as a model of the metabolic events in Alzheimer’s disease. Int J Dev Neuroscience 19(3):263–277CrossRefGoogle Scholar
  79. Kurosawa M, Sato A, Sato Y (1989) Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats. Neurosci Lett 98:45–50PubMedCrossRefGoogle Scholar
  80. Lamour Y, Dutar P, Jobert A (1984) Cortical projections of the nucleus of the diagonal band of Broca and of the substantia innominata in the rat: an anatomical study using the anterograde transport of a conjugate of wheat germ agglutinin and horseradish peroxidase. Neuroscience 12:395–408PubMedCrossRefGoogle Scholar
  81. Leanza G, Nilsson OG, Wiley RG, Björklund A (1995) Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur J Neuroscience 7(2):329–343CrossRefGoogle Scholar
  82. Lelkes Z, Porkka-Heiskanen T, Stenberg D (2013) Cholinergic basal forebrain structures are involved in the mediation of the arousal effect of noradrenaline. J Sleep Res 22(6):721–726PubMedCrossRefGoogle Scholar
  83. Levey AI (1993) Immunological localization of m1‐m5 muscarinic acetylcholine receptors in peripheral tissues and brain. Life Sci 52:441–448PubMedCrossRefGoogle Scholar
  84. Levin ED (1992) Nicotinic systems and cognitive function. Psychopharmacology 108:417–431PubMedCrossRefGoogle Scholar
  85. Liu Y, Zeng X, Hui Y et al (2015) Activation of α7 nicotinic acetylcholine receptors protects astrocytes against oxidative stress-induced apoptosis: implications for Parkinson’s disease. Neuropharmacology 91:87–96PubMedCrossRefGoogle Scholar
  86. Loewi O (1921) Über humorale Übertragbarkeit der Herznervenwirkung. Pflügers Arch Ges Physiol 189:239–242CrossRefGoogle Scholar
  87. Loup F, Tribollet E, Dubois-Dauphin M, Dreifuss JJ (1991) Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res 555(2):220–232PubMedCrossRefGoogle Scholar
  88. Macht DI (1923) A pharmacodynamic analysis of the cerebral effects of atropin, homatropin, scopolamin and related drugs. J Pharmacol Exp Ther 22:35–48Google Scholar
  89. MacIntosh F.C., Oboring P. E. (1955) Release of acetylcholine from the intact cerebral cortex. Abstr 19th Int Physiol Congr 580–581Google Scholar
  90. Malin DH, Novy BJ, Lett-Brown AE, Plotner RE, May BT, Radulescu SJ, Crothers MK, Osgood LD, Lake JR (1992) Galanin attenuates retention of one-trial reward learning. Life Sci 50(13):939–944PubMedCrossRefGoogle Scholar
  91. Marighetto A, Durkin T, Toumane A, Lebrun C, Jaffard R (1989) Septal alpha-noradrenergic antagonism in vivo blocks the testing-induced activation of septo-hippocampal cholinergic neurones and produces a concomitant deficit in working memory performance of mice. Pharmacol Biochem Behav 34(3):553–558PubMedCrossRefGoogle Scholar
  92. Mesulam M (2004a) The cholinergic lesion of Alzheimer’s Disease: pivotal factor or side show? Learn Mem 11:43–49PubMedCrossRefGoogle Scholar
  93. Mesulam MM (2004b) The cholinergic innervation of the human cerebral cortex. Prog Brain Res 145:67–78PubMedCrossRefGoogle Scholar
  94. 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 10:1185–1201PubMedCrossRefGoogle Scholar
  95. Mishima K, Tsukikawa H, Inada K, Fujii M, Iwasaki K, Matsumoto Y, Abe K, Egawa T, Fujiwara M (2001) Ameliorative effect of vasopressin-(4–9) through vasopressin V(1A) receptor on scopolamine-induced impairments of rat spatial memory in the eight-arm radial maze. Eur J Pharmacol 427(1):43–52PubMedCrossRefGoogle Scholar
  96. Molnár Z, Soós K, Lengyel I, Penke B, Szegedi V, Budai D (2004) Enhancement of NMDA responses by beta-amyloid peptides in the hippocampus in vivo. NeuroReport 15:1649–1652PubMedCrossRefGoogle Scholar
  97. Moore H, Stuckman S, Sarter M, Bruno JP (1995) Stimulation of cortical acetylcholine efflux by FG 7142 measured with repeated microdialysis sampling. Synapse 21:324–331PubMedCrossRefGoogle Scholar
  98. Morón I, Ramírez-Lugo L, Ballesteros MA, Gutiérrez R, Miranda MI, Gallo M, Bermúdez-Rattoni F (2002) Differential effects of bicuculline and muscimol microinjections into the nucleus basalis magnocellularis in taste and place aversive memory formation. Behav Brain Res 134(1–2):425–431PubMedCrossRefGoogle Scholar
  99. Mufson EJ, Cochran E, Benzing W, Kordower JH (1993) Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer’s disease and Down’s syndrome. Dementia 4(5):237–50PubMedGoogle Scholar
  100. Neugroschl J, Wang S (2011) Alzheimer’s disease: diagnosis and treatment across the spectrum of disease severity. Mt Sinai J Med 78(4):596–612PubMedPubMedCentralCrossRefGoogle Scholar
  101. Ogasawara T, Itoh Y, Tamura M, Mushiroi T, Ukai Y, Kise M, Kimura K (1999) Involvement of cholinergic and GABAergic systems in the reversal of memory disruption by NS-105, a cognition enhancer. Pharmacol Biochem Behav 64(1):41–52PubMedCrossRefGoogle Scholar
  102. Ogren SO, Hökfelt T, Kask K, Langel U, Bartfai T (1992) Evidence for a role of the neuropeptide galanin in spatial learning. Neuroscience 51(1):1–5PubMedCrossRefGoogle Scholar
  103. Page KJ, Saha A, Everitt BJ (1993) Differential activation and survival of basal forebrain neurons following infusions of excitatory amino acids: studies with the immediate early gene c-fos. Exp Brain Res 93:412–422PubMedGoogle Scholar
  104. Palmer AM, DeKosky ST (1993) Monoamine neurons in aging and Alzheimer’s disease. J Neural Transm Gen Sect 91:135–159PubMedCrossRefGoogle Scholar
  105. Pascual M, Pérez-Sust P, Soriano E (2004) The GABAergic septohippocampal pathway in control and reeler mice: target specificity and termination onto Reelin-expressing interneurons. Mol Cell Neurosci 25(4):679–691PubMedCrossRefGoogle Scholar
  106. Perry EK, Morris CM, Court JA, Cheng A, Fairbairn AF, McKeith IG et al (1995) Alteration in nicotine binding sites in Parkinson’s disease, Lewy body dementia and Alzheimer’s disease: possible index of early neuropathology. Neuroscience 64(2):385–395PubMedCrossRefGoogle Scholar
  107. Porkka-Heiskanen T, Strecker RE, McCarley RW (2000) Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study. Neuroscience 99:507–517PubMedCrossRefGoogle Scholar
  108. Querfurth HW, LaFerla FM (2010) Alzheimer’s disease. N Engl J Med 362(4):329–344PubMedCrossRefGoogle Scholar
  109. Ragozzino ME, Brown HD (2013) Muscarinic Cholinergic Receptor Agonists and Antagonists. Encyclopedia of Psychopharmacology. Springer, Berlin Heidelberg, pp 1–6Google Scholar
  110. Rangani RJ, Upadhya MA, Nakhate KT, Kokare DM, Subhedar NK (2012) Nicotine evoked improvement in learning and memory is mediated through NPY Y1 receptors in rat model of Alzheimer’s disease. Peptides 33(2):317–328PubMedCrossRefGoogle Scholar
  111. Rasmusson DD, Clow K, Szerb JC (1994) Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience 60(3):665–677PubMedCrossRefGoogle Scholar
  112. Rasmusson DD, Szerb IC, Jordan JL (1996) Differential effects of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and N-methyl-d-aspartate receptor antagonists applied to the basal forebrain on cortical acetylcholine release and electroencephalogram desynchronization. Neuroscience 72:419–427PubMedCrossRefGoogle Scholar
  113. Ribeiro-da-Silva A, Hökfelt T (2000) Neuroanatomical localisation of Substance P in the CNS and sensory neurons. Neuropeptides 34:256–271PubMedCrossRefGoogle Scholar
  114. Robinson JK, Crawley JN (1993a) Intraseptal galanin potentiates scopolamine impairment of delayed nonmatching to sample. J Neurosci 13(12):5119–5125PubMedGoogle Scholar
  115. Robinson JK, Crawley JN (1993b) Intraventricular galanin impairs delayed nonmatching-to sample performance in rats. Behav Neurosci 107(3):458–467PubMedCrossRefGoogle Scholar
  116. Saper CB (1984) Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 222:313–342PubMedCrossRefGoogle Scholar
  117. Scatton B, Bartholini G (1982) Gamma-Aminobutyric acid (GABA) receptor stimulation. IV. Effect of progabide (SL 76002) and other GABAergic agents on acetylcholine turnover in rat brain areas. J Pharmacol Exp Ther 220:689–695PubMedGoogle Scholar
  118. Semba K (2004) Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervation of the cerebral cortex. Prog Brain Res 145:3–43PubMedGoogle Scholar
  119. Sim JA, Griffith WH (1996) Muscarinic inhibition of glutamatergic transmissions onto rat magnocellular basal forebrain neurons in a thin-slice preparation. Eur J Neurosci 8:880–891PubMedCrossRefGoogle Scholar
  120. Smiley JF, Mesulam MM (1999) Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: an electron microscopic investigation in the monkey. Neuroscience 88:241–255PubMedCrossRefGoogle Scholar
  121. Smith CG, Beninger RJ, Mallet PE, Jhamandas K, Boegman RJ (1994) Basal forebrain injections of the benzodiazepine partial inverse agonist FG 7142 enhance memory of rats in the double Y-maze. Brain Res 666:61–67PubMedCrossRefGoogle Scholar
  122. Stanley EM, Fadel JR (2011) Aging-related alterations in orexin/hypocretin modulation of septohippocampal amino acid neurotransmission. Neuroscience 195:70–79PubMedPubMedCentralCrossRefGoogle Scholar
  123. Stäubli U, Huston JP (1980) Facilitation of learning by post-trial injection of substance P into the medial septal nucleus. Behav Brain Res 1:245–255PubMedCrossRefGoogle Scholar
  124. Stefani MR, Gold PE (1998) Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Res 813(1):50–56PubMedCrossRefGoogle Scholar
  125. Sundström E, Archer T, Melander T, Hökfelt T (1988) Galanin impairs acquisition but not retrieval of spatial memory in rats studied in the Morris swim maze. Neurosci Lett 88(3):331–335PubMedCrossRefGoogle Scholar
  126. Tanabe S, Shishido Y, Nakayama Y, Furushiro M, Hashimoto S, Terasaki T, Tsujimoto G, Yokokura T (1999) Effects of arginine-vasopressin fragment 4–9 on rodent cholinergic systems. Pharmacol Biochem Behav 63(4):549–553PubMedCrossRefGoogle Scholar
  127. Tansey EM (1991) Chemical neurotransmission in the autonomic nervous system: Sir Henry Dale and acetylcholine. Clin Auton Res 1:63–72PubMedCrossRefGoogle Scholar
  128. Torres EM, Perry TA, Blockland A, Wilkinson LS, Wiley RG, Lappi DA, Dunnet SB (1994) Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63(1):95–122PubMedCrossRefGoogle Scholar
  129. Tóth A, Hajnik T, Záborszky L, Détári L (2007) Effect of basal forebrain neuropeptide Y administration on sleep and spontaneous behavior in freely moving rats. Brain Res Bull 72(4–6):293–301PubMedCrossRefGoogle Scholar
  130. Ukai M, Miura M, Kameyama T (1995) Effects of galanin on passive avoidance response, elevated plus-maze learning, and spontaneous alternation performance in mice. Peptides 16(7):1283–1286PubMedCrossRefGoogle Scholar
  131. Weiss JH, Yin HZ, Choi DW (1994) Basal forebrain cholinergic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity. Neuroscience 60:659–664PubMedCrossRefGoogle Scholar
  132. Wettstein JG, Earley B, Junien JL (1995) Central nervous system pharmacology of neuropeptide Y. Pharmacol Ther 65(3):397–414PubMedCrossRefGoogle Scholar
  133. Winters BD, Dunnett SB (2004) Selective lesioning of the cholinergic septo-hippocampal pathway does not disrupt spatial short-term memory: a comparison with the effects of fimbria-fornix lesions. Behav Neurosci 118(3):546–562PubMedCrossRefGoogle Scholar
  134. Yakel JL (2014) Functional distribution and regulation of neuronal nicotinic ach receptors in the mammalian brain. In: Lester RAJ (ed) Nicotinic Receptors. Springer, New York, pp 93–114Google Scholar
  135. Yang C, Franciosi S, Brown RE (2013) Adenosine inhibits the excitatory synaptic inputs to Basal forebrain cholinergic, GABAergic, and parvalbumin neurons in mice. Front Neurol 4:77PubMedPubMedCentralCrossRefGoogle Scholar
  136. Záborszky L, Cullinan WE, Braun A (1991) Afferents to basal forebrain cholinergic projection neurons: an update. Adv Exp Med Biol 295:43–100PubMedCrossRefGoogle Scholar
  137. Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE (1997) Cortical input to the basal forebrain. Neuroscience 79:1051–1078PubMedCrossRefGoogle Scholar
  138. Záborszky L, Pang K, Somogyi J, Nadasdy Z, Kallo I (1999) The basal forebrain corticopetal system revisited. Ann N Y Acad Sci 877:339–367PubMedCrossRefGoogle Scholar
  139. Zaborszky L., Duque A., Gielow M., et al (2015) Organization of the basal forebrain cholinergic projection system: specific or diffuse?. Rat Nerv. Syst. (Fourth Edition)—Chapter 19CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Facultad de Medicina UBA, CONICET. ParaguayInstituto de Fisiología y Biofísica Bernardo HoussayBuenos AiresArgentina
  2. 2.Laboratorio de Neurofarmacología de la Memoria, Cátedra de FarmacologíaFacultad de Farmacia y Bioquímica, UBA. JunínBuenos AiresArgentina

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