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Neuromodulation by Glutamate and Acetylcholine can Change Circuit Dynamics by Regulating the Relative Influence of Afferent Input and Excitatory Feedback

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Abstract

Substances such as acetylcholine and glutamate act as both neurotransmitters and neuromodulators. As neuromodulators, they change neural information processing by regulating synaptic transmitter release, altering baseline membrane potential and spiking activity, and modifying long-term synaptic plasticity. Slice physiology research has demonstrated that many neuromodulators differentially modulate afferent, incoming information compared to intrinsic and recurrent processing in cortical structures such as piriform cortex, neocortex, and the hippocampus. The enhancement of afferent (external) pathways versus the suppression at recurrent (internal) pathways could cause cortical dynamics to switch between a predominant influence of external stimulation to a predominant influence of internal recall. Modulation of afferent versus intrinsic processing could contribute to the role of neuromodulators in regulating attention, learning, and memory effects in behavior.

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References

  1. Tseng G-F, Haberly LB (1988) Characterization of synaptically mediated fast and slow inhibitory processes in piriform cortex in an in vitro slice preparation. J Neurophysiol 59:1352–1376

    PubMed  CAS  Google Scholar 

  2. Lacaille JC, Schwartzkroin PA (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J Neurosci 8:1400–1410

    PubMed  CAS  Google Scholar 

  3. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA1 pyramidal neurons in vitro. J Physiol 354:319–331

    PubMed  CAS  Google Scholar 

  4. Giocomo LM, Hasselmo M (2005) Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus. Eur J Neurosci 22:1349–1356

    PubMed  Google Scholar 

  5. Mitchell SJ, Silver RA (2000) Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404:498–502

    PubMed  CAS  Google Scholar 

  6. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630–634

    PubMed  CAS  Google Scholar 

  7. Descarries L, Gisiger V, Steriade M (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurbiol 53:603–625

    CAS  Google Scholar 

  8. Umbriaco D, Garcia S, Beaulieu C, Descarries L (1995) Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5:605–620

    PubMed  CAS  Google Scholar 

  9. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK (1994) Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351–373

    PubMed  CAS  Google Scholar 

  10. Hasselmo ME, Bower JM (1992) Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 67:1222–1229

    PubMed  CAS  Google Scholar 

  11. Williams SH, Constanti A (1988) Quantitative effects of some muscarinic agonists on evoked surface-negative field potentials recorded from the guinea-pig olfactory cortex slice. Br J Pharmacol 93:846–854

    PubMed  CAS  Google Scholar 

  12. 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 

  13. Hounsgaard J (1978) Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 62:787–797

    PubMed  CAS  Google Scholar 

  14. Valentino RJ, Dingledine R (1981) Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1:784–792

    PubMed  CAS  Google Scholar 

  15. Vidal C, Changeux JP (1993) Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience 56:23–32

    PubMed  CAS  Google Scholar 

  16. Brocher S, Artola A, Singer W (1992) Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res 573:27–36

    PubMed  CAS  Google Scholar 

  17. Koerner JF, Cotman CW (1981) Micromolar l-2-amino-4-phosphonobutyric acid selectively inhibits perforant path synapses from lateral entorhinal cortex. Brain Res 216:192–198

    PubMed  CAS  Google Scholar 

  18. Yamamoto C, Kawai N (1967) Presynaptic action of acetylcholine in thin sections from the guinea pig dentate gyrus in vitro. Exp Neurol 19:176–187

    PubMed  CAS  Google Scholar 

  19. Kahle JS, Cotman CW (1989) Carbachol depresses synaptic responses in the medial but not the lateral perforant path. Brain Res 482:159–163

    PubMed  CAS  Google Scholar 

  20. Dutar P, Nicoll RA (1988) Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J Neurosci 8:4214–4224

    PubMed  CAS  Google Scholar 

  21. Hounsgaard J (1978) Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 62:787–797

    PubMed  CAS  Google Scholar 

  22. Hasselmo ME, Fehlau BP (2001) Differences in time course of ACh and GABA modulation of excitatory synaptic potentials in slices of rat hippocampus. J Neurophysiol 86:1792–1802

    PubMed  CAS  Google Scholar 

  23. Vogt KE, Regehr WG (2001) Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21:75–83

    PubMed  CAS  Google Scholar 

  24. Kremin TE, Hasselmo ME (2007) Cholinergic suppression of glutamatergic synaptic transmission in hippocampus region CA3 exhibits laminar selectivity: implications for hippocampal network dynamics. Neuroscience (in press)

  25. Kremin T et al (2006) Muscarinic suppression in stratum radiatum of CA1 shows dependence on presynaptic M1 receptors and is not dependent on effects at GABA(B) receptors. Neurobiol Learn Mem 85:153–163

    PubMed  CAS  Google Scholar 

  26. Hsieh CY, Cruikshank SJ, Metherate R (2000) Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res 880:51–64

    Google Scholar 

  27. Gil Z, Conners BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679–686

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  29. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075–7083

    PubMed  CAS  Google Scholar 

  30. Gioanni Y et al (1999) Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalmo-cortical transmission. Eur J Neurosci 11:18–30

    PubMed  CAS  Google Scholar 

  31. Barazangi N, Role LW (2001) Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. J Neurophysiol 86:463–474

    PubMed  CAS  Google Scholar 

  32. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716

    PubMed  CAS  Google Scholar 

  33. Choidini FC, Tassonya E, Hulo S, Brertrand D, Muller D (1999) Modulation of synaptic transmission by nicotine and nicotinic antagonists in hippocampus. Brain Res Bull 48:623–628

    Google Scholar 

  34. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075–7083

    PubMed  CAS  Google Scholar 

  35. Maggi L, Le Magueresse C, Changeux JP, Cherubini E (2003) Nicotine activates immature “silent” connections in the developing hippocampus. Proc Natl Acad Sci USA 100:2059–2064

    PubMed  CAS  Google Scholar 

  36. Girod R, Barazandi N, McGehee DS, Role LW (2000) Facilitation of glutamatergic neurotransmission by presynaptic nicotinic acetylcholine receptors. Neuropharmacology 39:2715–2725

    PubMed  CAS  Google Scholar 

  37. Hasselmo ME, Bower JM (1991) Selective suppression of afferent but not intrinsic fiber synaptic transmission by 2-amino-4-phosphonobutyric acid (AP4) in piriform cortex. Brain Res 548:248–255

    PubMed  CAS  Google Scholar 

  38. Tan Y, Hori N, Carpenter DO (2006) Electrophysiological effects of three groups of glutamate metabotropic receptors in rat piriform cortex. Cell Mol Neurobiol 26(4–6):915–924

    PubMed  CAS  Google Scholar 

  39. Capogna M (2004) Distinct properties of presynaptic group II and III metabotropic glutamate receptor-mediated inhibition of perforant pathway-CA1 EPSCs. Eur J Neurosci 19:2847–2858

    PubMed  Google Scholar 

  40. Giocomo LM, Hasselmo M (2006) Difference in time course of suppression of synaptic transmission by group II versus group III metabotropic glutamate receptors in region CA1 of the hippocampus. Hippocampus 16:1004–1016

    PubMed  CAS  Google Scholar 

  41. Burke JP, Hablitz JJ (1994) Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J Neurosci 14:5120–5130

    PubMed  CAS  Google Scholar 

  42. Gereau RW, Conn PJ (1995) Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15:6879–6889

    PubMed  CAS  Google Scholar 

  43. Vignes M et al (1995) Pharmacological evidence for an involvement of group II and group III mGluRs in the presynaptic regulation of excitatory synaptic responses in the CA1 region of rat hippocampal slices. Neuropharmacology 34:973–982

    PubMed  CAS  Google Scholar 

  44. Manzoni OJ, Castillo PE, Nicoll RA (1995) Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacology 34:965–971

    PubMed  CAS  Google Scholar 

  45. Dietrich D et al (1997) Metabotropic glutamate receptors modulate synaptic transmission in the perforant path: pharmacology and localization of two distinct receptors. Brain Res 767:220–227

    PubMed  CAS  Google Scholar 

  46. Hasselmo ME, Bower JM (1991) Selective suppression of afferent but not intrinsic fiber synaptic transmission by 2-amino-4-phophonobutyric acid (AP4) in piriform cortex. Brain Res 548:248–255

    PubMed  CAS  Google Scholar 

  47. Kew JNC, Ducarre JM, Pfimlin MC, Mutel V, Kemp JA (2001) Activity-dependent presynaptic autoinhibition by group II metabotropic glutamate receptors at the perforant path inputs to the dentate gyrus and CA1. Neuropharmacology 40:20–27

    PubMed  CAS  Google Scholar 

  48. Shigemoto R et al (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503–7522

    PubMed  CAS  Google Scholar 

  49. Flor PJ, Battaglia G, Nicoletti F, Gasparini F, Bruno V (2002) Neuroprotective activity of metabotropic glutamate receptor ligands. Adv Exp Med Biol 513:197–223

    PubMed  CAS  Google Scholar 

  50. Best AR, Thompson JV, Flietcher ML, Wilson DA (2005) Cortical metabotropic glutamate receptors contribute to habituation of a simple odor evoked behavior. J Neurosci 25:2513–2517

    PubMed  CAS  Google Scholar 

  51. Patil MM, Hasselmo ME (1999) Modulation of inhibitory synaptic potentials in the piriform cortex. J Neurophysiol 81(5):2103–2118

    PubMed  CAS  Google Scholar 

  52. McCormick DA, Prince DA (1985) Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci USA 82:6344–6348

    PubMed  CAS  Google Scholar 

  53. Pitler TA, Alger BE (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450:127–142

    PubMed  CAS  Google Scholar 

  54. Chapman CA, Lacaille JC (1999) Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci 19:8637–8645

    PubMed  CAS  Google Scholar 

  55. Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122–4132

    PubMed  CAS  Google Scholar 

  56. Cole AE, Nicoll RA (1984) The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res 305:283–290

    PubMed  CAS  Google Scholar 

  57. Widmer H, Ferrigan L, Davies CH, Cobb SR (2006) Evoked slow muscarinic acetylcholine synaptic potentials in rat hippocampal interneurons. Hippocampus 16:617–628

    PubMed  CAS  Google Scholar 

  58. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006) Cell type-specific dependence of muscarinic signaling in mouse hippocampal stratum oriens interneurons. J Physiol 570:595–610

    PubMed  CAS  Google Scholar 

  59. Lawrence JJ, Grinspan ZM, Statland JM, McBain CJ (2006) Muscarinic receptor activation tunes mouse stratum oriens interneurons to amplify spike reliability. J Physiol 571:555–562

    PubMed  CAS  Google Scholar 

  60. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75–78

    PubMed  CAS  Google Scholar 

  61. Kawai H, Zago W, Berg DK (2002) Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 22:7903–7912

    PubMed  CAS  Google Scholar 

  62. Selina Mok MH, Kew JN (2006) Excitation of rat hippocampal interneurons via modulation of endogenous agonist activity at the alpha7 nicotinic ACh receptor. J Physiol 574:699–710

    Google Scholar 

  63. Alkondon M, Albuquerque EX (2001) Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86:3043–3055

    PubMed  CAS  Google Scholar 

  64. Jones S, Yakel JL (1997) Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol 504:603–610

    PubMed  CAS  Google Scholar 

  65. Alkondon M, Braga MF, Pereira EF, Maelicke A, Albuquerque EX (2000) alpha7 nicotinic acetylcholine receptors and modulation of GABAergic synaptic transmission in the hippocampus. Eur J Pharmacol 393:59–67

    PubMed  CAS  Google Scholar 

  66. McQuiston AR, Madison DV (1999) Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19:2887–2896

    PubMed  CAS  Google Scholar 

  67. Buhler AV, Dunwiddie TV (2002) Alpha7 nicotinic acetylcholine receptors on GABAergic interneurons evoke dendritic and somatic inhibition of hippocampal neurons. J Neurophysiol 87:548–557

    PubMed  CAS  Google Scholar 

  68. Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83:2682–2690

    PubMed  CAS  Google Scholar 

  69. Price CJ, Karayannis T, Pal BZ, Capogna M (2005) Group II and III mGluRs-mediated presynaptic inhibition of EPSCs recorded from hippocampal interneurons of CA1 stratum lacunosum moleculare. Neuropharmacology 49:45–56

    PubMed  CAS  Google Scholar 

  70. Kogo N et al (2004) Depression of GABAergic input to identified hippocampal neurons by group III metabotropic glutamate receptors in the rat. Eur J Neurosci 19:2727–2740

    PubMed  Google Scholar 

  71. Doherty JJ et al (2004) Metabotropic glutamate receptors modulate feedback inhibition in a developmentally regulated manner in rat dentate gyrus. J Physiol 561:395–401

    PubMed  CAS  Google Scholar 

  72. Conners BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302–1320

    Google Scholar 

  73. 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 

  74. Barkai E, Hasselmo ME (1994) Modulation of the input/output function of rat piriform cortex pyramidal cells. J Neurophysiol 72:644–658

    PubMed  CAS  Google Scholar 

  75. McCormick DA, Prince DA (1986) Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 375:169–194

    PubMed  CAS  Google Scholar 

  76. Cole AE, Nicoll RA (1984) Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (London) 352:173–188

    CAS  Google Scholar 

  77. Burgard EC, Sarvey JM (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116(1–2):34–39

    PubMed  CAS  Google Scholar 

  78. Huerta PT, Lisman JE (1993) Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364(6439):723–725

    PubMed  CAS  Google Scholar 

  79. Hasselmo ME, Barkai E (1995) Cholinergic modulation of activity dependent synaptic plasticity in the piriform cortex and associative memory formation in a network biophysical simulation. J Neurosci 15:6592–6604

    PubMed  CAS  Google Scholar 

  80. Lin Y, Phillis JW (1991) Muscarinic agonist-mediated induction of long-term potentiation in rat. Brain Res 551:342–345

    PubMed  CAS  Google Scholar 

  81. Markram J, Segal M (1990) Acetylcholine potentiates responses to N-methyl-d-aspartate in the rat hippocampus. Neurosci Lett 113:62–65

    PubMed  CAS  Google Scholar 

  82. Markram H, Segal M (1990) Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol 427:381–393

    PubMed  CAS  Google Scholar 

  83. Rosati-Siri MD, Cattaneo A, Cherubini E (2006) Nicotine-induced enhancement of synaptic plasticity at CA3–CA1 synapses requires GABAergic interneurons in adult anti-NGF mice. J Physiol 576(17):361–377

    Google Scholar 

  84. Yamazaki Y, Jia Y, Hamaue N, Sumikawa K (2005) Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 22:845–860

    PubMed  Google Scholar 

  85. Holscher C (2002) Metabotropic glutamate receptors control gating of spike transmission in the hippocampus area CA1. Pharmacol Biochem Behav 73:307–316

    PubMed  CAS  Google Scholar 

  86. Riedel G, Wetzel W, Reymann KG (1996) Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiat 20:761–789

    CAS  Google Scholar 

  87. Bortolotto ZA, Fitzjohn SM, Collingridge GL (1999) Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 9:299–304

    PubMed  CAS  Google Scholar 

  88. Rush AM, Kilbride J, Rowan MJ, Anwyl R (2002) Presynaptic group III mGluR modulation of short-term plasticity in the lateral perforant path of the dentate gyrus in vitro. Brain Res 952:38–43

    PubMed  CAS  Google Scholar 

  89. Poschel B, Wroblewska B, Heinemann U, Manahan-Vaughan D (2005) The metabotropic glutamate receptor mGluR3 is critically required for hippocampal long-term depression and modulates long-term potentiation in the dentate gyrus of freely moving rats. Cereb Cortex 15:1414–1423

    PubMed  Google Scholar 

  90. Ghoneim MM, Mewaldt SP (1975) Effects of diazepam and scopolamine on storage, retrieval and organizational processes in memory. Psychopharmacologia 44:257–262

    PubMed  CAS  Google Scholar 

  91. Peterson RC (1977) Scopolamine-induced learning failures in man. Psychopharmacologia 52:283–289

    Google Scholar 

  92. Beatty WW, Butters N, Janowsky DS (1986) Patterns of memory failure after scopolamine treatment: implications for cholinergic hypotheses of dementia. Behav Neural Biol 45:196–211

    PubMed  CAS  Google Scholar 

  93. Sherman SJ, Atri A, Hasselmo M, Stern CE, Howard MW (2003) Scopolamine impairs human recognition memory: data and modeling. Behav Neurosci 117:526–539

    PubMed  CAS  Google Scholar 

  94. Tang Y, Mishkin M, Aigner TG (1997) Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci USA 94:12667–12669

    PubMed  CAS  Google Scholar 

  95. Damasio AR, Graff-Redford NR, Eslinger PJ et al (1985) Amnesia following basal forebrain lesions. Arch Neurol 42:263–271

    PubMed  CAS  Google Scholar 

  96. DeLuca J, Cicerone KD (1991) Confabulation following aneurysm of the anterior communicating artery. Cortex 27:417–423

    PubMed  CAS  Google Scholar 

  97. DeLuca J (1993) Predicting neurobehavioral patterns following anterior communicating artery aneurysm. Cortex 29:639–647

    PubMed  CAS  Google Scholar 

  98. Heilman KM, Sypert GW (1977) Korsakoff’s syndrome resulting from bilateral fornix lesions. Neurology 27:490–493

    PubMed  CAS  Google Scholar 

  99. Hodges JR, Carpenter K (1991) Anterograde amnesia with fornix damage following removal of IIIrd ventricle colloid cyst. J Neurol Neurosurg Psychiatr 54:633–638

    Article  PubMed  CAS  Google Scholar 

  100. Tucker DM, Roeltgen DP, Tully R, Hartmann J, Boxell C (1988) Memory dysfunction following unilateral transection of the fornix: a hippocampal disconnection syndrome. Cortex 24:465–472

    PubMed  CAS  Google Scholar 

  101. Rogers JL, Kesner RP (2003) Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol Learn Mem 80:332–345

    PubMed  CAS  Google Scholar 

  102. Winters BD, Saksida LM, Bussey TJ (2006) Paradoxical facilitation of object recognition memory after infusion of scopolamine into perirhinal cortex: implications for cholinergic system function. J Neurosci 26:9520–9529

    PubMed  CAS  Google Scholar 

  103. Chang Q, Savage LM, Gold PE (2006) Microdialysis measures of functional increases in ACh release in the hippocampus with and without inclusion of acetylcholinesterase inhibitors in the perfusate. J Neurochem 97:697–706

    PubMed  CAS  Google Scholar 

  104. Pych JC, Chang Q, Colon-Rivera C, Haag R, Gold PE (2005) Acetylcholine release in the hippocampus and striatum during place and response training. Learn Mem 12:564–572

    PubMed  Google Scholar 

  105. Ghonheim MM, Mewaldt SP (1975) Effects of diazepam and scopolamine on storage, retrieval and organization processes in memory. Psychopharmacologia 44:257–262

    Google Scholar 

  106. Crow TJ, Grove-White IG (1973) An analysis of the learning deficit following hyoscine administration to man. Br J Pharmacol 49:322–327

    PubMed  CAS  Google Scholar 

  107. Flicker C, Serby M, Ferris SH (1990) Scopolamine effects on memory, language, visuospatial praxis and psychomotor speed. Psychopharm 100:243–250

    CAS  Google Scholar 

  108. Liljequist R, Mattila MJ (1979) Effect of physostigmine and scopolamine on the memory functioning of chess players. Med Biol 51:402–405

    Google Scholar 

  109. Ostfeld AM, Aruguete A (1962) Central nervous system effects of hyoscine in man. J Pharmacol Exp Ther 137:133–139

    PubMed  CAS  Google Scholar 

  110. Drachman DA, Leavitt J (1974) Human memory and the cholinergic system. Arch Neurol 30:113–121

    PubMed  CAS  Google Scholar 

  111. Aigner TG, Mishkin M (1986) The effects of physostigmine and scopolamine on recognition memory in monkeys. Behav Neurosci 45:81–87

    CAS  Google Scholar 

  112. Aigner TG, Walker DL, Mishkin M (1991) Comparison of the effects of scopolamine administered before and after acquisition in a test of visual recognition memory in monkeys. Behav Neural Biol 55:61–67

    PubMed  CAS  Google Scholar 

  113. Besheer J, Short KR, Bevins RA (2001) Dopaminergic and cholinergic antagonist in a novel-object detection task with rats. Behav Brain Res 126:211–217

    PubMed  CAS  Google Scholar 

  114. Atri A et al (2004) Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behav Neurosci 118:223–236

    PubMed  CAS  Google Scholar 

  115. De Rosa E, Hasselmo ME (2000) Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci 114:32–41

    PubMed  Google Scholar 

  116. Broks P et al (1988) Modeling dementia: effects of scopolamine on memory and attention. Neuropsychologia 26:685–700

    PubMed  CAS  Google Scholar 

  117. Caine ED, Weingartner H, Ludlow CL, Cudahy EA, Wehry S (1981) Qualitative analysis of scopolamine-induced amnesia. Psychopharm 74:74–80

    CAS  Google Scholar 

  118. Whishaw IQ (1985) Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav Neurosci 99:979–1005

    PubMed  CAS  Google Scholar 

  119. Buresova O, Bolhuis JJ, Bures J (1986) Differential effects of cholinergic blockade on performance of rats in the water tank navigation task and in a radial water maze. Behav Neurosci 100:476–482

    PubMed  CAS  Google Scholar 

  120. Cassel JC, Kelche C (1989) Scopolamine treatment and fimbria–fornix lesions: mimetic effects on radial maze performance. Physiol Behav 46(3):347–353

    PubMed  CAS  Google Scholar 

  121. Bolhuis JJ, Strijkstra AM, Kramers RJ (1988) Effects of scopolamine on performance of rats in a delayed-response radial maze task. Physiol Behav 43:403–409

    PubMed  CAS  Google Scholar 

  122. Berry SD, Thompson RF (1979) Medial septal lesions retard classical conditioning of the nicitating membrane response in rabbits. Science 205(4402):209–211

    PubMed  CAS  Google Scholar 

  123. Solomon PR, Solomon SD, Schaaf EV, Perry HE (1983) Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 20:329–331

    Google Scholar 

  124. Solomon PR et al (1993) Disruption of human eyeblink conditioning after central cholinergic blockade with scopolamine. Behav Neurosci 107:271–279

    PubMed  CAS  Google Scholar 

  125. Seager MA, Asaka Y, Berry SD (1999) Scopolamine disruption of behavioral and hippocampal responses in appetitive trace classical conditioning. Behav Brain Res 100:143–151

    PubMed  CAS  Google Scholar 

  126. Young SL, Bohenek DL, Fanselow MS (1995) Scopolamine impairs acquisition and facilitates consolidation of fear conditioning: differential effects for tone vs. context conditioning. Neurobiol Learn Mem 63(2):174–180

    PubMed  CAS  Google Scholar 

  127. Rogers JL, Kesner RP (2004) Cholinergic modulation of the hippocampus during encoding and retrieval of tone/shock-induced fear conditioning. Learn Mem 11:102–107

    PubMed  Google Scholar 

  128. Wesnes K, Warburton DM (1983) Effects of scopolamine on stimulus sensitivity and response bias in a visual vigilance task. Neuropsychobiol 9:154–157

    Article  CAS  Google Scholar 

  129. Wesnes K, Warburton DM (1984) Effects of scopolamine and nicotine on human rapid information processing performance. Psychopharmacol 82:147–150

    CAS  Google Scholar 

  130. Wesnes K, Revell A (1984) The separate and combined effects of scopolamine and nicotine on human information processing. Psychopharm 84:5–11

    CAS  Google Scholar 

  131. McGurk SR, Levin ED, Butcher LL (1991) Impairment of radial-arm maze performance in rats following lesions involving the cholinergic medial pathway: reversal by arecoline and differential effects of muscarinic and nicotinic antagonists. Neuroscience 44:137–147

    PubMed  CAS  Google Scholar 

  132. Rusted JM, Warburton DM (1992) Facilitation of memory by post-trial administration of nicotine—evidence for an attentional explanation. Psychopharmacology 108:452–455

    PubMed  CAS  Google Scholar 

  133. Levin ED et al (1998) Transdermal nicotine effects on attention. Psychopharmacology 140:135–141

    PubMed  CAS  Google Scholar 

  134. Manusco G, Warburton DM, Melen M, Sherwood N, Tirelli E (1999) Selective effects of nicotine on attentional processes. Psychopharmacology 146:199–204

    Google Scholar 

  135. Warburton DM, Ruster JM, Muller C (1992) Patterns of facilitation of memory by nicotine. Behav Pharmacol 3:375–378

    PubMed  CAS  Google Scholar 

  136. Phillips S, Fox P (1998) An investigation into the effects of nicotine gum on short-term memory. Psychopharmacology 140:429–433

    PubMed  CAS  Google Scholar 

  137. Warburton DM, Skinner A, Martin CD (2001) Improved incidental memory with nicotine after semantic processing but not after phonological processing. Psychopharmacology 153:258–263

    PubMed  CAS  Google Scholar 

  138. Colrain IM, Mangan GL, Pellett OL, Bates TC (1992) Effects of post-learning smoking on memory consolidation. Psychopharmacology (Berl) 108:448–451

    CAS  Google Scholar 

  139. Poltavski DV, Petros T (2005) Effects of transdermal nicotine on prose memory and attention in smokers and nonsmokers. Physiol Behav 83:833–843

    PubMed  CAS  Google Scholar 

  140. Warburton DM, Rusted JM, Fowler J (1992) A comparison of the attentional and consolidation hypothesis for the facilitation of memory by nicotine. Psychopharmacology (Berl) 108:443–447

    CAS  Google Scholar 

  141. Mangan GL, Golding JF (1983) The effects of smoking on memory consolidation. J Psychol 115:65–77

    PubMed  CAS  Google Scholar 

  142. Elrod K, Buccafusco JJ, Jackson WJ (1988) Nicotine enhances delayed matching-to-sample performance by primates. Life Sci 43:277–287

    PubMed  CAS  Google Scholar 

  143. Socci DJ, Sanberg PR, Arendash GW (1995) Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol Aging 16:857–860

    PubMed  CAS  Google Scholar 

  144. Puma C, Deschaux O, Molimard R, Bizot JC (1999) Nicotine improves memory in an object recognition task in rats. Eur Neuropsychopharmacol 9:323–327

    PubMed  CAS  Google Scholar 

  145. Arendash GW, Sanberg PR, Sengstock GJ (1995) Nicotine enhances the learning and memory of aged rats. Pharmacol Biochem Behav 52:517–523

    PubMed  CAS  Google Scholar 

  146. Marti Barros D, Ramirez MR, Dos Reis EA, Izquierdo I (2006) Participation of hippocampal nicotinic receptors in acquisition, consolidation and retrieval of memory for one trial inhibitory avoidance in rats. Neuroscience 126:651–656

    Google Scholar 

  147. Levin ED, Kaplan S, Boardman A (1997) Acute nicotine interactions with nicotinic muscarinic antagonists: working and reference memory effects in the 16-arm radial maze. Behav Pharmacol 8:236–242

    PubMed  CAS  Google Scholar 

  148. Levin ED, Simon BB (1998) Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology 138:217–230

    PubMed  CAS  Google Scholar 

  149. Levin ED, Castonguay M, Ellison GD (1987) Effects of nicotinic receptor blocker mecamylamine on radial-arm maze performance in rats. Behav Neural Biol 48:206–212

    PubMed  CAS  Google Scholar 

  150. Gould TJ, Lommock JA (2003) Nicotine enhances contextual fear conditioning and ameliorates ethanol-induced deficits in contextual fear conditioning. Behav Neurosci 117:1276–1282

    PubMed  CAS  Google Scholar 

  151. Gould TJ, Stephen Higgins J (2003) Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training. Neurobiol Learn Mem 80:147–157

    PubMed  CAS  Google Scholar 

  152. Nott A, Levin ED (2006) Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory. Brain Res 1081:72–78

    PubMed  CAS  Google Scholar 

  153. Muir JL, Everitt BJ, Robbins TW (1995) Reversal of visual attentional dysfunction following lesions of the cholinergic basal forebrain by physostigmine and nicotine but not by the 5-HT3 receptor antagonist, ondansetron. Psychopharmacology (Berl) 118:82–92

    CAS  Google Scholar 

  154. Whitehouse PJ, Au KS (1986) Cholinergic receptors in aging and Alzheimer’s disease. Prog Neuropsychopharmacol Biol Psychiatry 10:665–676

    PubMed  CAS  Google Scholar 

  155. Newhouse PA, Potter A, Levin ED (1997) Nicotinic systems and Alzheimer’s disease: implications for therapeutics. Drug Aging 11:206–228

    CAS  Google Scholar 

  156. Kametani H, Kawamura H (1990) Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis. Life Sci 47:421–426

    PubMed  CAS  Google Scholar 

  157. Marrosu F et al (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep–wake cycle in freely moving cats. Brain Res 671:329–332

    PubMed  CAS  Google Scholar 

  158. Bland BH, Colom LV (1993) Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41:157–208

    PubMed  CAS  Google Scholar 

  159. Arnold HM, Burk JA, Hodgson EM, Sarter M, Bruno JP (2002) Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience 114:451–460

    PubMed  CAS  Google Scholar 

  160. Himmelheber AM, Sarter M, Bruno JP (2001) The effects of manipulations of attentional demand on cortical acetylcholine release. Brain Res Cogn Brain Res 12:353–370

    PubMed  CAS  Google Scholar 

  161. Chrobak JJ, Buzsaki G (1994) Selective activation of deep layer (V–VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14:6160–6170

    PubMed  CAS  Google Scholar 

  162. Steriade M (1994) Sleep oscillations and their blockage by activating systems. J Psychiatry Neurosci 19:354–358

    PubMed  CAS  Google Scholar 

  163. Gais S, Born J (2004) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci USA 101:2140–2144

    PubMed  CAS  Google Scholar 

  164. Rasch BH, Born J, Gais S (2006) Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J Cogn Neurosci 18:793–802

    PubMed  Google Scholar 

  165. Bergink V, Van Megen HJGM, Westenberg HGM (2004) Glutamate and anxiety. Eur Neuropsychopharmacology 14:175–183

    CAS  Google Scholar 

  166. Chojnacka-Wojcik E, Klodzinska A, Pilc A (2001) Glutamate receptor ligands as anxiolytics. Curr Opin Investig Drugs 2:1112–1119

    PubMed  CAS  Google Scholar 

  167. Tatarczynska E et al (2002) Anxiolytic and antidepressant like effects of group III metabotropic glutamate agonist (1S,3R,4S)-1-aminocyclopentane-1,3,4-tricarboxylic acid (ACPT-I) in rats. Pol J Pharmacol 54:707–710

    PubMed  CAS  Google Scholar 

  168. Linden AM et al (2002) Increased anxiety-related behavior in mice deficient for metabotropic glutamate 8 (mGluR8) receptor. Neuropharmacology 43:251–259

    PubMed  CAS  Google Scholar 

  169. Linden AM, Baez M, Bergeron M, Schoepp DD (2003) Increased C-FOS expression in the centromedial nucleus of the thalamus in metabotropic glutamate 8 receptor knockout mice following the elevated plus-maze test. Neuroscience 121:167–178

    PubMed  CAS  Google Scholar 

  170. Folbergrova J et al (2005) Seizures induced in immature rats by homocysteic acid and the associated brain damage are prevented by group II metabotropic glutamate receptor agonist (2R,4R)-4-aminopyrrolidine-2,4-dicarboxylate. Exp Neurol 192:420–436

    PubMed  CAS  Google Scholar 

  171. Movsesyan VA, Faden AI (2006) Neuroprotective effects of selective group II mGluR activation in brain trauma and traumatic neuronal injury. J Neurotrauma 23:117–127

    PubMed  Google Scholar 

  172. Riedel G, Wetzel W, Reymann KG (1994) (R,S)-alpha-methyl-4-carboxyphenylglycine (MCPG) blocks spatial learning in rats and long-term potentiation in the dentate gyrus in vivo. Neurosci Lett 167:141–144

    PubMed  CAS  Google Scholar 

  173. Riedel G, Wetzel W, Kozikowski AP, Reymann KG (1995) Block of spatial learning by mGluR agonist tADA in rats. Neuropharmacology 34:559–561

    PubMed  CAS  Google Scholar 

  174. Pettit HO, Lutz D, Gutierrez C, Eveleth D (1994) I.C.V. infusions of ACPD attenuate learning in a Morris water maze paradigm. Neurosci Lett 178:43–46

    PubMed  CAS  Google Scholar 

  175. Holscher C et al (2004) Lack of metabotropic glutamate receptor subtype 7 selectively impairs short-term working memory but not long-term memory. Behav Brain Res 154:473–481

    PubMed  CAS  Google Scholar 

  176. Best AR, Wilson DA (2004) Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J Neurosci 24:652–660

    PubMed  CAS  Google Scholar 

  177. Riedel G, Harrington NR, Kozikowski AP, Sandager-Nielsen K, Macphail EM (2002) Variation of CS salience reveals group II mGluR-dependent and independent forms of conditioning in the rat. Neurpharmacology 43:205–214

    CAS  Google Scholar 

  178. Baker GR, Bashir ZI, Brown MW, Warburton EC (2006) A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory. Learn Mem 13:178–186

    Google Scholar 

  179. Car H, Wisniewska RJ, Wisniewski K (2004) 2R,4R-APDC influence on hypoxia-induced impairment of learning and memory processes in passive avoidance test. Pol J Pharmacol 56:527–537

    PubMed  CAS  Google Scholar 

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Acknowledgements

Work supported by NIMH MH60013, NIH DA16454 (Program for Collaborative Research in Computational Neuroscience-CRCNS), NSF Science of Learning Center SBE-0354378 and Silvio O. Conte Center Grant MH71750.

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Correspondence to Michael E. Hasselmo.

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Giocomo, L.M., Hasselmo, M.E. Neuromodulation by Glutamate and Acetylcholine can Change Circuit Dynamics by Regulating the Relative Influence of Afferent Input and Excitatory Feedback. Mol Neurobiol 36, 184–200 (2007). https://doi.org/10.1007/s12035-007-0032-z

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