Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline

Neuron

Volumn 91, Issue 6, 2016, Pages 1199-1218

  Ballinger, Elizabeth C ^a   Ananth, Mala ^b   Talmage, David A ^b   Role, Lorna W ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINERGIC RECEPTOR; GLUTAMATE RECEPTOR 1; ACETYLCHOLINE;

ALZHEIMER DISEASE; ATTENTION; BASAL FOREBRAIN; CELL STRUCTURE; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONNECTOME; ENZYME RELEASE; FIRING RATE; HUMAN; LONG TERM POTENTIATION; MEMORY; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE PROJECTION; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SHORT TERM DEPRESSION; SYNAPTIC TRANSMISSION; ANIMAL; COGNITION; CYTOLOGY; NERVE TRACT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACETYLCHOLINE; ANIMALS; BASAL FOREBRAIN; CHOLINERGIC NEURONS; COGNITION; COGNITION DISORDERS; HUMANS; NEURAL PATHWAYS;

EID: 84991229359     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.09.006     Document Type: Review

References (209)

1. Aarsland, D., Mosimann, U.P., McKeith, I.G., Role of cholinesterase inhibitors in Parkinson's disease and dementia with Lewy bodies. J. Geriatr. Psychiatry Neurol. 17 (2004), 164–171.
2. Backus, A.R., Schoffelen, J.M., Szebényi, S., Hanslmayr, S., Doeller, C.F., Hippocampal-prefrontal theta oscillations support memory integration. Curr. Biol. 26 (2016), 450–457.
3. Barnstedt, O., Owald, D., Felsenberg, J., Brain, R., Moszynski, J.P., Talbot, C.B., Perrat, P.N., Waddell, S., Memory-relevant mushroom body output synapses are cholinergic. Neuron 89 (2016), 1237–1247.
4. Bartus, R.T., Dean, R.L. 3rd, Beer, B., Lippa, A.S., The cholinergic hypothesis of geriatric memory dysfunction. Science 217 (1982), 408–414.
5. Beierlein, M., Synaptic properties and functional consequences of cholinergic signalling in the mammalian CNS. J. Physiol. 592 (2014), 4129–4130.
6. Bentley, P., Driver, J., Dolan, R.J., Cholinesterase inhibition modulates visual and attentional brain responses in Alzheimer's disease and health. Brain 131 (2008), 409–424.
7. Bloem, B., Schoppink, L., Rotaru, D.C., Faiz, A., Hendriks, P., Mansvelder, H.D., van de Berg, W.D., Wouterlood, F.G., Topographic mapping between basal forebrain cholinergic neurons and the medial prefrontal cortex in mice. J. Neurosci. 34 (2014), 16234–16246.
8. Blusztajn, J.K., Rinnofner, J., Intrinsic cholinergic neurons in the hippocampus: fact or artifact?. Front. Synaptic Neurosci., 8, 2016, 6.
9. Bohnen, N.I., Müller, M.L., Kotagal, V., Koeppe, R.A., Kilbourn, M.R., Gilman, S., Albin, R.L., Frey, K.A., Heterogeneity of cholinergic denervation in Parkinson's disease without dementia. J. Cereb. Blood Flow Metab. 32 (2012), 1609–1617.
10. Bohnen, N.I., Albin, R.L., Müller, M.L., Petrou, M., Kotagal, V., Koeppe, R.A., Scott, P.J., Frey, K.A., Frequency of cholinergic and caudate nucleus dopaminergic deficits across the predemented cognitive spectrum of Parkinson disease and evidence of interaction effects. JAMA Neurol. 72 (2015), 194–200.
11. Boskovic, Z., Alfonsi, F., Rumballe, B.A., Fonseka, S., Windels, F., Coulson, E.J., The role of p75NTR in cholinergic basal forebrain structure and function. J. Neurosci. 34 (2014), 13033–13038.
12. Bracco, L., Bessi, V., Padiglioni, S., Marini, S., Pepeu, G., Do cholinesterase inhibitors act primarily on attention deficit? A naturalistic study in Alzheimer's disease patients. J. Alzheimers Dis. 40 (2014), 737–742.
13. Brown, D.A., Muscarinic acetylcholine receptors (mAChRs) in the nervous system: some functions and mechanisms. J. Mol. Neurosci. 41 (2010), 340–346.
14. Buchanan, K.A., Petrovic, M.M., Chamberlain, S.E., Marrion, N.V., Mellor, J.R., Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 68 (2010), 948–963.
15. Burgess, N., Maguire, E.A., O'Keefe, J., The human hippocampus and spatial and episodic memory. Neuron 35 (2002), 625–641.
16. Butcher, A.J., Bradley, S.J., Prihandoko, R., Brooke, S.M., Mogg, A., Bourgognon, J.M., Macedo-Hatch, T., Edwards, J.M., Bottrill, A.R., Challiss, R.A., et al. An antibody biosensor establishes the activation of the m1 muscarinic acetylcholine receptor during learning and memory. J. Biol. Chem. 291 (2016), 8862–8875.
17. Carli, M., Luschi, R., Samanin, R., Dose-related impairment of spatial learning by intrahippocampal scopolamine: antagonism by ondansetron, a 5-HT3 receptor antagonist. Behav. Brain Res. 82 (1997), 185–194.
18. Celebi, O., Temuçin, C.M., Elibol, B., Saka, E., Short latency afferent inhibition in Parkinson's disease patients with dementia. Mov. Disord. 27 (2012), 1052–1055.
19. Chandler, D., Waterhouse, B.D., Evidence for broad versus segregated projections from cholinergic and noradrenergic nuclei to functionally and anatomically discrete subregions of prefrontal cortex. Front. Behav. Neurosci., 6, 2012, 20.
20. Chandler, D.J., Lamperski, C.S., Waterhouse, B.D., Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex. Brain Res. 1522 (2013), 38–58.
21. Chavez, C., Zaborszky, L., Basal forebrain cholinergic-auditory cortical network: primary versus nonprimary auditory cortical areas. Cereb. Cortex, 2016, 10.1093/cercor/bhw091 Published online April 12, 2016.
22. Chen, H., Huang, X., Guo, X., Mailman, R.B., Park, Y., Kamel, F., Umbach, D.M., Xu, Q., Hollenbeck, A., Schatzkin, A., Blair, A., Smoking duration, intensity, and risk of Parkinson disease. Neurology 74 (2010), 878–884.
23. Chen, L., Chatterjee, M., Li, J.Y., The mouse homeobox gene Gbx2 is required for the development of cholinergic interneurons in the striatum. J. Neurosci. 30 (2010), 14824–14834.
24. Chen, N., Sugihara, H., Sur, M., An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nat. Neurosci. 18 (2015), 892–902.
25. Cheng, Q., Yakel, J.L., Presynaptic α7 nicotinic acetylcholine receptors enhance hippocampal mossy fiber glutamatergic transmission via PKA activation. J. Neurosci. 34 (2014), 124–133.
26. Cheng, Q., Yakel, J.L., The effect of α7 nicotinic receptor activation on glutamatergic transmission in the hippocampus. Biochem. Pharmacol. 97 (2015), 439–444.
27. Choi, S.H., Jung, T.M., Lee, J.E., Lee, S.K., Sohn, Y.H., Lee, P.H., Volumetric analysis of the substantia innominata in patients with Parkinson's disease according to cognitive status. Neurobiol. Aging 33 (2012), 1265–1272.
28. Cobb, S.R., Davies, C.H., Cholinergic modulation of hippocampal cells and circuits. J. Physiol. 562 (2005), 81–88.
29. Cohen, M.R., Maunsell, J.H., Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12 (2009), 1594–1600.
30. Colgin, L.L., Denninger, T., Fyhn, M., Hafting, T., Bonnevie, T., Jensen, O., Moser, M.B., Moser, E.I., Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462 (2009), 353–357.
31. Cui, X., Weng, Y.Q., Frappé, I., Burgess, A., Girão da Cruz, M.T., Schachner, M., Aubert, I., The cell adhesion molecule L1 regulates the expression of choline acetyltransferase and the development of septal cholinergic neurons. Brain Behav. 1 (2011), 73–86.
32. Dani, J.A., Bertrand, D., Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47 (2007), 699–729.
33. Dannenberg, H., Pabst, M., Braganza, O., Schoch, S., Niediek, J., Bayraktar, M., Mormann, F., Beck, H., Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks. J. Neurosci. 35 (2015), 8394–8410.
34. Descarries, L., Mechawar, N., Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Prog. Brain Res. 125 (2000), 27–47.
35. Descarries, L., Gisiger, V., Steriade, M., Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol. 53 (1997), 603–625.
36. Dickinson, J.A., Kew, J.N., Wonnacott, S., Presynaptic alpha 7- and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol. Pharmacol. 74 (2008), 348–359.
37. Douchamps, V., Jeewajee, A., Blundell, P., Burgess, N., Lever, C., Evidence for encoding versus retrieval scheduling in the hippocampus by theta phase and acetylcholine. J. Neurosci. 33 (2013), 8689–8704.
38. Drachman, D.A., Leavitt, J., Human memory and the cholinergic system. A relationship to aging?. Arch. Neurol. 30 (1974), 113–121.
39. Dubois, B., Tolosa, E., Katzenschlager, R., Emre, M., Lees, A.J., Schumann, G., Pourcher, E., Gray, J., Thomas, G., Swartz, J., et al. Donepezil in Parkinson's disease dementia: a randomized, double-blind efficacy and safety study. Mov. Disord. 27 (2012), 1230–1238.
40. Duffy, A.M., Zhou, P., Milner, T.A., Pickel, V.M., Spatial and intracellular relationships between the alpha7 nicotinic acetylcholine receptor and the vesicular acetylcholine transporter in the prefrontal cortex of rat and mouse. Neuroscience 161 (2009), 1091–1103.
41. Düzel, E., Penny, W.D., Burgess, N., Brain oscillations and memory. Curr. Opin. Neurobiol. 20 (2010), 143–149.
42. Easton, A., Douchamps, V., Eacott, M., Lever, C., A specific role for septohippocampal acetylcholine in memory?. Neuropsychologia 50 (2012), 3156–3168.
43. Elshatory, Y., Gan, L., The LIM-homeobox gene Islet-1 is required for the development of restricted forebrain cholinergic neurons. J. Neurosci. 28 (2008), 3291–3297.
44. Eyjolfsdottir, H., Eriksdotter, M., Linderoth, B., Lind, G., Juliusson, B., Kusk, P., Almkvist, O., Andreasen, N., Blennow, K., Ferreira, D., et al. Targeted delivery of nerve growth factor to the cholinergic basal forebrain of Alzheimer's disease patients: application of a second-generation encapsulated cell biodelivery device. Alzheimers Res. Ther., 8, 2016, 30.
45. Fabian-Fine, R., Skehel, P., Errington, M.L., Davies, H.A., Sher, E., Stewart, M.G., Fine, A., Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J. Neurosci. 21 (2001), 7993–8003.
46. Frotscher, M., Vida, I., Bender, R., Evidence for the existence of non-GABAergic, cholinergic interneurons in the rodent hippocampus. Neuroscience 96 (2000), 27–31.
47. Galloway, C.R., Lebois, E.P., Shagarabi, S.L., Hernandez, N.A., Manns, J.R., Effects of selective activation of M1 and M4 muscarinic receptors on object recognition memory performance in rats. Pharmacology 93 (2014), 57–64.
48. Galvez, B., Gross, N., Sumikawa, K., Activation of α7 nicotinic acetylcholine receptors protects potentiated synapses from depotentiation during theta pattern stimulation in the hippocampal CA1 region of rats. Neuropharmacology 105 (2016), 378–387.
49. Geula, C., Mesulam, M.M., Cortical cholinergic fibers in aging and Alzheimer's disease: a morphometric study. Neuroscience 33 (1989), 469–481.
50. Giraldez-Perez, R.M., Gaytan, S.P., Pasaro, R., Cholinergic and nitrergic neuronal networks in the goldfish telencephalon. Acta Neurobiol. Exp. (Warsz.) 73 (2013), 338–353.
51. Goard, M., Dan, Y., Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12 (2009), 1444–1449.
52. Goldberg, J.A., Ding, J.B., Surmeier, D.J., Muscarinic modulation of striatal function and circuitry. Handb. Exp. Pharmacol. 208 (2012), 223–241.
53. Gonzales, K.K., Smith, Y., Cholinergic interneurons in the dorsal and ventral striatum: anatomical and functional considerations in normal and diseased conditions. Ann. N Y Acad. Sci. 1349 (2015), 1–45.
54. Gotti, C., Zoli, M., Clementi, F., Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol. Sci. 27 (2006), 482–491.
55. Gould, R.W., Dencker, D., Grannan, M., Bubser, M., Zhan, X., Wess, J., Xiang, Z., Locuson, C., Lindsley, C.W., Conn, P.J., Jones, C.K., Role for the M1 Muscarinic Acetylcholine Receptor in Top-Down Cognitive processing using a touchscreen visual discrimination task in mice. ACS Chem. Neurosci. 6 (2015), 1683–1695.
56. Granger, A.J., Mulder, N., Saunders, A., Sabatini, B.L., Cotransmission of acetylcholine and GABA. Neuropharmacology 100 (2016), 40–46.
57. Gritti, I., Henny, P., Galloni, F., Mainville, L., Mariotti, M., Jones, B.E., Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience 143 (2006), 1051–1064.
58. Gritton, H.J., Howe, W.M., Mallory, C.S., Hetrick, V.L., Berke, J.D., Sarter, M., Cortical cholinergic signaling controls the detection of cues. Proc. Natl. Acad. Sci. USA 113 (2016), E1089–E1097.
59. Grothe, M., Zaborszky, L., Atienza, M., Gil-Neciga, E., Rodriguez-Romero, R., Teipel, S.J., Amunts, K., Suarez-Gonzalez, A., Cantero, J.L., Reduction of basal forebrain cholinergic system parallels cognitive impairment in patients at high risk of developing Alzheimer's disease. Cereb. Cortex 20 (2010), 1685–1695.
60. Grothe, M., Heinsen, H., Teipel, S.J., Atrophy of the cholinergic Basal forebrain over the adult age range and in early stages of Alzheimer's disease. Biol. Psychiatry 71 (2012), 805–813.
61. Gu, Z., Yakel, J.L., Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71 (2011), 155–165.
62. Gu, Z., Lamb, P.W., Yakel, J.L., Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J. Neurosci. 32 (2012), 12337–12348.
63. Guillem, K., Bloem, B., Poorthuis, R.B., Loos, M., Smit, A.B., Maskos, U., Spijker, S., Mansvelder, H.D., Nicotinic acetylcholine receptor β2 subunits in the medial prefrontal cortex control attention. Science 333 (2011), 888–891.
64. Halff, A.W., Gómez-Varela, D., John, D., Berg, D.K., A novel mechanism for nicotinic potentiation of glutamatergic synapses. J. Neurosci. 34 (2014), 2051–2064.
65. Hall, H., Reyes, S., Landeck, N., Bye, C., Leanza, G., Double, K., Thompson, L., Halliday, G., Kirik, D., Hippocampal Lewy pathology and cholinergic dysfunction are associated with dementia in Parkinson's disease. Brain 137 (2014), 2493–2508.
66. Hanyu, H., Asano, T., Sakurai, H., Tanaka, Y., Takasaki, M., Abe, K., MR analysis of the substantia innominata in normal aging, Alzheimer disease, and other types of dementia. AJNR Am. J. Neuroradiol. 23 (2002), 27–32.
67. Hascup, K.N., Hascup, E.R., Soluble amyloid-beta42 stimulates glutamate release through activation of the alpha7 nicotinic acetylcholine receptor. J. Alzheimers Dis. 53 (2016), 337–347.
68. Hasselmo, M.E., Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 2013, 20120523.
69. Hasselmo, M.E., Sarter, M., Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36 (2011), 52–73.
70. Hasselmo, M.E., Stern, C.E., Theta rhythm and the encoding and retrieval of space and time. Neuroimage 85 (2014), 656–666.
71. Hawrylycz, M.J., Lein, E.S., Guillozet-Bongaarts, A.L., Shen, E.H., Ng, L., Miller, J.A., van de Lagemaat, L.N., Smith, K.A., Ebbert, A., Riley, Z.L., et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489 (2012), 391–399.
72. Higley, M.J., Picciotto, M.R., Neuromodulation by acetylcholine: examples from schizophrenia and depression. Curr. Opin. Neurobiol. 29 (2014), 88–95.
73. Hong, E., Santhakumar, K., Akitake, C.A., Ahn, S.J., Thisse, C., Thisse, B., Wyart, C., Mangin, J.M., Halpern, M.E., Cholinergic left-right asymmetry in the habenulo-interpeduncular pathway. Proc. Natl. Acad. Sci. USA 110 (2013), 21171–21176.
74. Howe, W.M., Berry, A.S., Francois, J., Gilmour, G., Carp, J.M., Tricklebank, M., Lustig, C., Sarter, M., Prefrontal cholinergic mechanisms instigating shifts from monitoring for cues to cue-guided performance: converging electrochemical and fMRI evidence from rats and humans. J. Neurosci. 33 (2013), 8742–8752.
75. Hu, J., Zhu, C., Liu, Y., Wang, F., Huang, Z., Fan, W., Wu, J., Dynamic alterations of gene expression of nicotinic acetylcholine receptor α7, α4 and β2 subunits in an acute MPTP-lesioned mouse model. Neurosci. Lett. 494 (2011), 232–236.
76. Hyde, M., Choueiry, J., Smith, D., de la Salle, S., Nelson, R., Impey, D., Baddeley, A., Aidelbaum, R., Millar, A., Knott, V., Cholinergic modulation of auditory P3 event-related potentials as indexed by CHRNA4 and CHRNA7 genotype variation in healthy volunteers. Neurosci. Lett. 623 (2016), 36–41.
77. Janak, P.H., Tye, K.M., From circuits to behaviour in the amygdala. Nature 517 (2015), 284–292.
78. Jennings, K.A., Platt, N.J., Cragg, S.J., The impact of a parkinsonian lesion on dynamic striatal dopamine transmission depends on nicotinic receptor activation. Neurobiol. Dis. 82 (2015), 262–268.
79. Jia, Z., Guo, Y., Tang, Y., Xu, Q., Li, B., Wu, Q., Regulation of the protocadherin Celsr3 gene and its role in globus pallidus development and connectivity. Mol. Cell. Biol. 34 (2014), 3895–3910.
80. Jiang, L., Emmetsberger, J., Talmage, D.A., Role, L.W., Type III neuregulin 1 is required for multiple forms of excitatory synaptic plasticity of mouse cortico-amygdala circuits. J. Neurosci. 33 (2013), 9655–9666.
81. Jiang, L., López-Hernández, G.Y., Lederman, J., Talmage, D.A., Role, L.W., Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system. Rev. Neurosci. 25 (2014), 755–771.
82. Jiang, L., Kundu, S., Lederman, J.D., López-Hernández, G.Y., Ballinger, E.C., Wang, S., Talmage, D.A., Role, L.W., Cholinergic Signaling Controls Conditioned Fear Behaviors and Enhances Plasticity of Cortical-Amygdala Circuits. Neuron 90 (2016), 1057–1070.
83. Jung, Y., Hsieh, L.S., Lee, A.M., Zhou, Z., Coman, D., Heath, C.J., Hyder, F., Mineur, Y.S., Yuan, Q., Goldman, D., et al. An epigenetic mechanism mediates developmental nicotine effects on neuronal structure and behavior. Nat. Neurosci. 19 (2016), 905–914.
84. Kalmbach, A., Waters, J., Modulation of high- and low-frequency components of the cortical local field potential via nicotinic and muscarinic acetylcholine receptors in anesthetized mice. J. Neurophysiol. 111 (2014), 258–272.
85. Kalmbach, A., Hedrick, T., Waters, J., Selective optogenetic stimulation of cholinergic axons in neocortex. J. Neurophysiol. 107 (2012), 2008–2019.
86. Katsuki, F., Constantinidis, C., Bottom-up and top-down attention: different processes and overlapping neural systems. Neuroscientist 20 (2014), 509–521.
87. Kihara, T., Shimohama, S., Urushitani, M., Sawada, H., Kimura, J., Kume, T., Maeda, T., Akaike, A., Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity. Brain Res. 792 (1998), 331–334.
88. Kim, J.H., Jung, A.H., Jeong, D., Choi, I., Kim, K., Shin, S., Kim, S.J., Lee, S.H., Selectivity of Neuromodulatory Projections from the Basal Forebrain and Locus Ceruleus to Primary Sensory Cortices. J. Neurosci. 36 (2016), 5314–5327.
89. Klein, J.C., Eggers, C., Kalbe, E., Weisenbach, S., Hohmann, C., Vollmar, S., Baudrexel, S., Diederich, N.J., Heiss, W.D., Hilker, R., Neurotransmitter changes in dementia with Lewy bodies and Parkinson disease dementia in vivo. Neurology 74 (2010), 885–892.
90. 123I]iododexetimide binding to cortical muscarinic receptors in unilaterally 6-hydroxydopamine lesioned rats. Nucl. Med. Biol. 41 (2014), 90–95.
91. Knott, V., Choueiry, J., Dort, H., Smith, D., Impey, D., de la Salle, S., Philippe, T., Baseline-dependent modulating effects of nicotine on voluntary and involuntary attention measured with brain event-related P3 potentials. Pharmacol. Biochem. Behav. 122 (2014), 107–117.
92. Knott, V., de la Salle, S., Choueiry, J., Impey, D., Smith, D., Smith, M., Beaudry, E., Saghir, S., Ilivitsky, V., Labelle, A., Neurocognitive effects of acute choline supplementation in low, medium and high performer healthy volunteers. Pharmacol. Biochem. Behav. 131 (2015), 119–129.
93. Knox, D., The role of basal forebrain cholinergic neurons in fear and extinction memory. Neurobiol. Learn. Mem. 133 (2016), 39–52.
94. Knox, D., Keller, S.M., Cholinergic neuronal lesions in the medial septum and vertical limb of the diagonal bands of Broca induce contextual fear memory generalization and impair acquisition of fear extinction. Hippocampus 26 (2016), 718–726.
95. Kondo, H., Zaborszky, L., Topographic organization of the basal forebrain projections to the perirhinal, postrhinal, and entorhinal cortex in rats. J. Comp. Neurol. 524 (2016), 2503–2515.
96. Koukouli, F., Maskos, U., The multiple roles of the α7 nicotinic acetylcholine receptor in modulating glutamatergic systems in the normal and diseased nervous system. Biochem. Pharmacol. 97 (2015), 378–387.
97. Kucinski, A., Sarter, M., Modeling Parkinson's disease falls associated with brainstem cholinergic systems decline. Behav. Neurosci. 129 (2015), 96–104.
98. Kucinski, A., Paolone, G., Bradshaw, M., Albin, R.L., Sarter, M., Modeling fall propensity in Parkinson's disease: deficits in the attentional control of complex movements in rats with cortical-cholinergic and striatal-dopaminergic deafferentation. J. Neurosci. 33 (2013), 16522–16539.
99. Kuhl, D.E., Minoshima, S., Fessler, J.A., Frey, K.A., Foster, N.L., Ficaro, E.P., Wieland, D.M., Koeppe, R.A., In vivo mapping of cholinergic terminals in normal aging, Alzheimer's disease, and Parkinson's disease. Ann. Neurol. 40 (1996), 399–410.
100. Kunec, S., Hasselmo, M.E., Kopell, N., Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. J. Neurophysiol. 94 (2005), 70–82.
101. Kutlu, M.G., Gould, T.J., Nicotinic modulation of hippocampal cell signaling and associated effects on learning and memory. Physiol. Behav. 155 (2016), 162–171.
102. Laursen, B., Mørk, A., Plath, N., Kristiansen, U., Bastlund, J.F., Cholinergic degeneration is associated with increased plaque deposition and cognitive impairment in APPswe/PS1dE9 mice. Behav. Brain Res. 240 (2013), 146–152.
103. Lee, J.E., Cho, K.H., Song, S.K., Kim, H.J., Lee, H.S., Sohn, Y.H., Lee, P.H., Exploratory analysis of neuropsychological and neuroanatomical correlates of progressive mild cognitive impairment in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 85 (2014), 7–16.
104. Lilja, A.M., Porras, O., Storelli, E., Nordberg, A., Marutle, A., Functional interactions of fibrillar and oligomeric amyloid-β with alpha7 nicotinic receptors in Alzheimer's disease. J. Alzheimers Dis. 23 (2011), 335–347.
105. Liu, S., Ninan, I., Antonova, I., Battaglia, F., Trinchese, F., Narasanna, A., Kolodilov, N., Dauer, W., Hawkins, R.D., Arancio, O., alpha-Synuclein produces a long-lasting increase in neurotransmitter release. EMBO J. 23 (2004), 4506–4516.
106. Liu, S., Fa, M., Ninan, I., Trinchese, F., Dauer, W., Arancio, O., Alpha-synuclein involvement in hippocampal synaptic plasticity: role of NO, cGMP, cGK and CaMKII. Eur. J. Neurosci. 25 (2007), 3583–3596.
107. Liu, Q., Xie, X., Emadi, S., Sierks, M.R., Wu, J., A novel nicotinic mechanism underlies β-amyloid-induced neurotoxicity. Neuropharmacology 97 (2015), 457–463.
108. Louis, E.D., Benito-León, J., Bermejo-Pareja, F., Neurological Disorders in Central Spain (NEDICES) Study Group. Population-based prospective study of cigarette smoking and risk of incident essential tremor. Neurology 70 (2008), 1682–1687.
109. Lu, C.B., Henderson, Z., Nicotine induction of theta frequency oscillations in rodent hippocampus in vitro. Neuroscience 166 (2010), 84–93.
110. Lubin, M., Erisir, A., Aoki, C., Ultrastructural immunolocalization of the alpha 7 nAChR subunit in guinea pig medial prefrontal cortex. Ann. N Y Acad. Sci. 868 (1999), 628–632.
111. Luchicchi, A., Bloem, B., Viaña, J.N., Mansvelder, H.D., Role, L.W., Illuminating the role of cholinergic signaling in circuits of attention and emotionally salient behaviors. Front. Synaptic Neurosci., 6, 2014, 24.
112. MacDermott, A.B., Role, L.W., Siegelbaum, S.A., Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci. 22 (1999), 443–485.
113. Magen, I., Fleming, S.M., Zhu, C., Garcia, E.C., Cardiff, K.M., Dinh, D., De La Rosa, K., Sanchez, M., Torres, E.R., Masliah, E., et al. Cognitive deficits in a mouse model of pre-manifest Parkinson's disease. Eur. J. Neurosci. 35 (2012), 870–882.
114. Marin, O., Anderson, S.A., Rubenstein, J.L., Origin and molecular specification of striatal interneurons. J. Neurosci. 20 (2000), 6063–6076.
115. Martinello, K., Huang, Z., Lujan, R., Tran, B., Watanabe, M., Cooper, E.C., Brown, D.A., Shah, M.M., Cholinergic afferent stimulation induces axonal function plasticity in adult hippocampal granule cells. Neuron 85 (2015), 346–363.
116. Mechawar, N., Watkins, K.C., Descarries, L., Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat. J. Comp. Neurol. 443 (2002), 250–258.
117. Mena-Segovia, J., Structural and functional considerations of the cholinergic brainstem. J Neural Transm (Vienna) 123 (2016), 731–736.
118. Mesulam, M.M., Mufson, E.J., Levey, A.I., Wainer, B.H., Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol. 214 (1983), 170–197.
119. Micheau, J., Marighetto, A., Acetylcholine and memory: a long, complex and chaotic but still living relationship. Behav. Brain Res. 221 (2011), 424–429.
120. Miloyan, B.H., Razani, J., Larco, A., Avila, J., Chung, J., Aspects of Attention predict real-world task performance in Alzheimer's disease. Appl. Neuropsychol. Adult, 2013, 10.1080/09084282.2012.685133 Published online February 13, 2013.
121. Mitchell, J.F., Sundberg, K.A., Reynolds, J.H., Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63 (2009), 879–888.
122. Mitsushima, D., Sano, A., Takahashi, T., A cholinergic trigger drives learning-induced plasticity at hippocampal synapses. Nat. Commun., 4, 2013, 2760.
123. Miwa, J.M., Lester, H.A., Walz, A., Optimizing cholinergic tone through lynx modulators of nicotinic receptors: implications for plasticity and nicotine addiction. Physiology (Bethesda) 27 (2012), 187–199.
124. Mufson, E.J., Counts, S.E., Che, S., Ginsberg, S.D., Neuronal gene expression profiling: uncovering the molecular biology of neurodegenerative disease. Prog. Brain Res. 158 (2006), 197–222.
125. Müller, M.L., Bohnen, N.I., Kotagal, V., Scott, P.J., Koeppe, R.A., Frey, K.A., Albin, R.L., Clinical markers for identifying cholinergic deficits in Parkinson's disease. Mov. Disord. 30 (2015), 269–273.
126. Muñoz, W., Rudy, B., Spatiotemporal specificity in cholinergic control of neocortical function. Curr. Opin. Neurobiol. 26 (2014), 149–160.
127. Nakano, I., Hirano, A., Parkinson's disease: neuron loss in the nucleus basalis without concomitant Alzheimer's disease. Ann. Neurol. 15 (1984), 415–418.
128. Nejad-Davarani, S., Muller, M., Koeppe, R., Scott, P., Dauer, W., Albin, R., Frey, K., Bohnen, N., Clinical correlation of multivariate spatial covariance analysis of 18F-FEOBV VAChT PET in Parkinson disease. J. Nucl. Med., 57, 2016 1832–1832.
129. Nelson, A., Mooney, R., The basal forebrain and motor cortex provide convergent yet distinct movement-related inputs to the auditory cortex. Neuron 90 (2016), 635–648.
130. Newhouse, P.A., Sunderland, T., Tariot, P.N., Weingartner, H., Thompson, K., Mellow, A.M., Cohen, R.M., Murphy, D.L., The effects of acute scopolamine in geriatric depression. Arch. Gen. Psychiatry 45 (1988), 906–912.
131. Newman, E.L., Gillet, S.N., Climer, J.R., Hasselmo, M.E., Cholinergic blockade reduces theta-gamma phase amplitude coupling and speed modulation of theta frequency consistent with behavioral effects on encoding. J. Neurosci. 33 (2013), 19635–19646.
132. Newman, E.L., Climer, J.R., Hasselmo, M.E., Grid cell spatial tuning reduced following systemic muscarinic receptor blockade. Hippocampus 24 (2014), 643–655.
133. Nguyen, H.N., Huppé-Gourgues, F., Vaucher, E., Activation of the mouse primary visual cortex by medial prefrontal subregion stimulation is not mediated by cholinergic basalo-cortical projections. Front. Syst. Neurosci., 9, 2015, 1.
134. Nichols, W.A., Henderson, B.J., Yu, C., Parker, R.L., Richards, C.I., Lester, H.A., Miwa, J.M., Lynx1 shifts α4β2 nicotinic receptor subunit stoichiometry by affecting assembly in the endoplasmic reticulum. J. Biol. Chem. 289 (2014), 31423–31432.
135. Niemegeers, P., Dumont, G.J., Quisenaerts, C., Morrens, M., Boonzaier, J., Fransen, E., de Bruijn, E.R., Hulstijn, W., Sabbe, B.G., The effects of nicotine on cognition are dependent on baseline performance. Eur. Neuropsychopharmacol. 24 (2014), 1015–1023.
136. Nordman, J.C., Kabbani, N., An interaction between α7 nicotinic receptors and a G-protein pathway complex regulates neurite growth in neural cells. J. Cell Sci. 125 (2012), 5502–5513.
137. Nordman, J.C., Phillips, W.S., Kodama, N., Clark, S.G., Del Negro, C.A., Kabbani, N., Axon targeting of the alpha 7 nicotinic receptor in developing hippocampal neurons by Gprin1 regulates growth. J. Neurochem. 129 (2014), 649–662.
138. Oddo, S., Caccamo, A., Green, K.N., Liang, K., Tran, L., Chen, Y., Leslie, F.M., LaFerla, F.M., Chronic nicotine administration exacerbates tau pathology in a transgenic model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 102 (2005), 3046–3051.
139. Padakanti, P.K., Zhang, X., Jin, H., Cui, J., Wang, R., Li, J., Flores, H.P., Parsons, S.M., Perlmutter, J.S., Tu, Z., In vitro and in vivo characterization of two C-11-labeled pet tracers for vesicular acetylcholine transporter. Mol. Imaging Biol. 16 (2014), 773–780.
140. Paolone, G., Angelakos, C.C., Meyer, P.J., Robinson, T.E., Sarter, M., Cholinergic control over attention in rats prone to attribute incentive salience to reward cues. J. Neurosci. 33 (2013), 8321–8335.
141. Parikh, V., Pomerleau, F., Huettl, P., Gerhardt, G.A., Sarter, M., Bruno, J.P., Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur. J. Neurosci. 20 (2004), 1545–1554.
142. Parikh, V., Kozak, R., Martinez, V., Sarter, M., Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56 (2007), 141–154.
143. Park, H.E., Park, I.S., Oh, Y.S., Yang, D.W., Lee, K.S., Choi, H.S., Ahn, K.J., Kim, J.S., Subcortical whiter matter hyperintensities within the cholinergic pathways of patients with dementia and parkinsonism. J. Neurol. Sci. 353 (2015), 44–48.
144. Perry, E.K., Morris, C.M., Court, J.A., Cheng, A., Fairbairn, A.F., McKeith, I.G., Irving, D., Brown, A., Perry, R.H., Alteration in nicotine binding sites in Parkinson's disease, Lewy body dementia and Alzheimer's disease: possible index of early neuropathology. Neuroscience 64 (1995), 385–395.
145. Petrou, M., Frey, K.A., Kilbourn, M.R., Scott, P.J., Raffel, D.M., Bohnen, N.I., Müller, M.L., Albin, R.L., Koeppe, R.A., In vivo imaging of human cholinergic nerve terminals with (-)-5-(18)F-fluoroethoxybenzovesamicol: biodistribution, dosimetry, and tracer kinetic analyses. J. Nucl. Med. 55 (2014), 396–404.
146. Picciotto, M.R., Higley, M.J., Mineur, Y.S., Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76 (2012), 116–129.
147. Pinto, L., Goard, M.J., Estandian, D., Xu, M., Kwan, A.C., Lee, S.H., Harrison, T.C., Feng, G., Dan, Y., Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16 (2013), 1857–1863.
148. Pisani, A., Bernardi, G., Ding, J., Surmeier, D.J., Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30 (2007), 545–553.
149. Pombero, A., Bueno, C., Saglietti, L., Rodenas, M., Guimera, J., Bulfone, A., Martinez, S., Pallial origin of basal forebrain cholinergic neurons in the nucleus basalis of Meynert and horizontal limb of the diagonal band nucleus. Development 138 (2011), 4315–4326.
150. Poorthuis, R.B., Bloem, B., Schak, B., Wester, J., de Kock, C.P., Mansvelder, H.D., Layer-specific modulation of the prefrontal cortex by nicotinic acetylcholine receptors. Cereb. Cortex 23 (2013), 148–161.
151. Possin, K.L., Kang, G.A., Guo, C., Fine, E.M., Trujillo, A.J., Racine, C.A., Wilheim, R., Johnson, E.T., Witt, J.L., Seeley, W.W., et al. Rivastigmine is associated with restoration of left frontal brain activity in Parkinson's disease. Mov. Disord. 28 (2013), 1384–1390.
152. Puddifoot, C.A., Wu, M., Sung, R.J., Joiner, W.J., Ly6h regulates trafficking of alpha7 nicotinic acetylcholine receptors and nicotine-induced potentiation of glutamatergic signaling. J. Neurosci. 35 (2015), 3420–3430.
153. Puzzo, D., Privitera, L., Leznik, E., Fà, M., Staniszewski, A., Palmeri, A., Arancio, O., Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 28 (2008), 14537–14545.
154. Quik, M., Perez, X.A., Bordia, T., Nicotine as a potential neuroprotective agent for Parkinson's disease. Mov. Disord. 27 (2012), 947–957.
155. Ray, N.J., Metzler-Baddeley, C., Khondoker, M.R., Grothe, M.J., Teipel, S., Wright, P., Heinsen, H., Jones, D.K., Aggleton, J.P., O'Sullivan, M.J., Cholinergic basal forebrain structure influences the reconfiguration of white matter connections to support residual memory in mild cognitive impairment. J. Neurosci. 35 (2015), 739–747.
156. Rinne, J.O., Kaasinen, V., Järvenpää, T., Någren, K., Roivainen, A., Yu, M., Oikonen, V., Kurki, T., Brain acetylcholinesterase activity in mild cognitive impairment and early Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 74 (2003), 113–115.
157. Rochester, L., Yarnall, A.J., Baker, M.R., David, R.V., Lord, S., Galna, B., Burn, D.J., Cholinergic dysfunction contributes to gait disturbance in early Parkinson's disease. Brain 135 (2012), 2779–2788.
158. Roland, J.J., Stewart, A.L., Janke, K.L., Gielow, M.R., Kostek, J.A., Savage, L.M., Servatius, R.J., Pang, K.C., Medial septum-diagonal band of Broca (MSDB) GABAergic regulation of hippocampal acetylcholine efflux is dependent on cognitive demands. J. Neurosci. 34 (2014), 506–514.
159. Romberg, C., Bussey, T.J., Saksida, L.M., Paying more attention to attention: towards more comprehensive cognitive translation using mouse models of Alzheimer's disease. Brain Res. Bull. 92 (2013), 49–55.
160. Runfeldt, M.J., Sadovsky, A.J., MacLean, J.N., Acetylcholine functionally reorganizes neocortical microcircuits. J. Neurophysiol. 112 (2014), 1205–1216.
161. ∗ nicotinic acetylcholine receptors using the novel specific radioligand (-)-[(18)F]Flubatine. Neuroimage 118 (2015), 199–208.
162. Salehi, A., Delcroix, J.D., Belichenko, P.V., Zhan, K., Wu, C., Valletta, J.S., Takimoto-Kimura, R., Kleschevnikov, A.M., Sambamurti, K., Chung, P.P., et al. Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 51 (2006), 29–42.
163. Sanchez-Ortiz, E., Yui, D., Song, D., Li, Y., Rubenstein, J.L., Reichardt, L.F., Parada, L.F., TrkA gene ablation in basal forebrain results in dysfunction of the cholinergic circuitry. J. Neurosci. 32 (2012), 4065–4079.
164. Saper, C.B., Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J. Comp. Neurol. 222 (1984), 313–342.
165. Sarter, M., Bruno, J.P., Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95 (2000), 933–952.
166. Sarter, M., Kim, Y., Interpreting chemical neurotransmission in vivo: techniques, time scales, and theories. ACS Chem. Neurosci. 6 (2015), 8–10.
167. Sarter, M., Lustig, C., Howe, W.M., Gritton, H., Berry, A.S., Deterministic functions of cortical acetylcholine. Eur. J. Neurosci. 39 (2014), 1912–1920.
168. Sarter, M., Lustig, C., Berry, A.S., Gritton, H., Howe, W.M., Parikh, V., What do phasic cholinergic signals do?. Neurobiol. Learn. Mem. 130 (2016), 135–141.
169. Sarter, M., Lustig, C., Blakely, R.D., Koshy Cherian, A., Cholinergic genetics of visual attention: Human and mouse choline transporter capacity variants influence distractibility. J. Physiol. Paris, 2016, 10.1016/j.jphysparis.2016.07.001 Published online July 9, 2016.
170. Shanmugasundaram, B., Sase, A., Miklosi, A.G., Sialana, F.J., Subramaniyan, S., Aher, Y.D., Gröger, M., Höger, H., Bennett, K.L., Lubec, G., Frontal cortex and hippocampus neurotransmitter receptor complex level parallels spatial memory performance in the radial arm maze. Behav. Brain Res. 289 (2015), 157–168.
171. Shin, J., Choi, S., Lee, J.E., Lee, H.S., Sohn, Y.H., Lee, P.H., Subcortical white matter hyperintensities within the cholinergic pathways of Parkinson's disease patients according to cognitive status. J. Neurol. Neurosurg. Psychiatry 83 (2012), 315–321.
172. Stanley, E.M., Wilson, M.A., Fadel, J.R., Hippocampal neurotransmitter efflux during one-trial novel object recognition in rats. Neurosci. Lett. 511 (2012), 38–42.
173. Subramaniyan, S., Heo, S., Patil, S., Li, L., Hoger, H., Pollak, A., Lubec, G., A hippocampal nicotinic acetylcholine alpha 7-containing receptor complex is linked to memory retrieval in the multiple-T-maze in C57BL/6j mice. Behav. Brain Res. 270 (2014), 137–145.
174. Sussel, L., Marin, O., Kimura, S., Rubenstein, J.L., Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126 (1999), 3359–3370.
175. Szegő, É.M., Gerhardt, E., Outeiro, T.F., Kermer, P., Dopamine-depletion and increased α-synuclein load induce degeneration of cortical cholinergic fibers in mice. J. Neurol. Sci. 310 (2011), 90–95.
176. Szegő, E.M., Outeiro, T.F., Kermer, P., Schulz, J.B., Impairment of the septal cholinergic neurons in MPTP-treated A30P α-synuclein mice. Neurobiol. Aging 34 (2013), 589–601.
177. Teipel, S.J., Flatz, W.H., Heinsen, H., Bokde, A.L., Schoenberg, S.O., Stöckel, S., Dietrich, O., Reiser, M.F., Möller, H.J., Hampel, H., Measurement of basal forebrain atrophy in Alzheimer's disease using MRI. Brain 128 (2005), 2626–2644.
178. Teipel, S.J., Meindl, T., Grinberg, L., Grothe, M., Cantero, J.L., Reiser, M.F., Möller, H.J., Heinsen, H., Hampel, H., The cholinergic system in mild cognitive impairment and Alzheimer's disease: an in vivo MRI and DTI study. Hum. Brain Mapp. 32 (2011), 1349–1362.
179. Thiele, A., Muscarinic signaling in the brain. Annu. Rev. Neurosci. 36 (2013), 271–294.
180. Thiele, A., Herrero, J.L., Distler, C., Hoffmann, K.P., Contribution of cholinergic and GABAergic mechanisms to direction tuning, discriminability, response reliability, and neuronal rate correlations in macaque middle temporal area. J. Neurosci. 32 (2012), 16602–16615.
181. Umbriaco, D., Watkins, K.C., Descarries, L., Cozzari, C., Hartman, B.K., Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J. Comp. Neurol. 348 (1994), 351–373.
182. Umbriaco, D., Garcia, S., Beaulieu, C., Descarries, L., Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5 (1995), 605–620.
183. Unal, C.T., Golowasch, J.P., Zaborszky, L., Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front. Behav. Neurosci., 6, 2012, 21.
184. Unal, C.T., Pare, D., Zaborszky, L., Impact of basal forebrain cholinergic inputs on basolateral amygdala neurons. J. Neurosci. 35 (2015), 853–863.
185. Wallace, T.L., Ballard, T.M., Pouzet, B., Riedel, W.J., Wettstein, J.G., Drug targets for cognitive enhancement in neuropsychiatric disorders. Pharmacol. Biochem. Behav. 99 (2011), 130–145.
186. Wallenstein, G.V., Vago, D.R., Intrahippocampal scopolamine impairs both acquisition and consolidation of contextual fear conditioning. Neurobiol. Learn. Mem. 75 (2001), 245–252.
187. Weintraub, D., Somogyi, M., Meng, X., Rivastigmine in Alzheimer's disease and Parkinson's disease dementia: an ADAS-cog factor analysis. Am. J. Alzheimers Dis. Other Demen. 26 (2011), 443–449.
188. Whitehouse, P.J., Struble, R.G., Clark, A.W., Price, D.L., Alzheimer disease: plaques, tangles, and the basal forebrain. Ann. Neurol., 12, 1982, 494.
189. Wisman, L.A., Sahin, G., Maingay, M., Leanza, G., Kirik, D., Functional convergence of dopaminergic and cholinergic input is critical for hippocampus-dependent working memory. J. Neurosci. 28 (2008), 7797–7807.
190. Woolf, N.J., Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37 (1991), 475–524.
191. Wu, M.N., He, Y.X., Guo, F., Qi, J.S., Alpha4beta2 nicotinic acetylcholine receptors are required for the amyloid beta protein-induced suppression of long-term potentiation in rat hippocampal CA1 region in vivo. Brain Res. Bull. 77 (2008), 84–90.
192. Wu, J., Ishikawa, M., Zhang, J., Hashimoto, K., Brain imaging of nicotinic receptors in Alzheimer's disease. Int. J. Alzheimers Dis., 2010, 2010, 548913.
193. Wu, H., Williams, J., Nathans, J., Complete morphologies of basal forebrain cholinergic neurons in the mouse. eLife, 3, 2014, e02444.
194. Wu, M., Puddifoot, C.A., Taylor, P., Joiner, W.J., Mechanisms of inhibition and potentiation of α4β2 nicotinic acetylcholine receptors by members of the Ly6 protein family. J. Biol. Chem. 290 (2015), 24509–24518.
195. Wu, J., Liu, Q., Tang, P., Mikkelsen, J.D., Shen, J., Whiteaker, P., Yakel, J.L., Heteromeric α7β2 Nicotinic Acetylcholine Receptors in the Brain. Trends Pharmacol. Sci. 37 (2016), 562–574.
196. Xu, W., Weissmiller, A.M., White, J.A. 2nd, Fang, F., Wang, X., Wu, Y., Pearn, M.L., Zhao, X., Sawa, M., Chen, S., et al. Amyloid precursor protein-mediated endocytic pathway disruption induces axonal dysfunction and neurodegeneration. J. Clin. Invest. 126 (2016), 1815–1833.
197. Yamasaki, M., Matsui, M., Watanabe, M., Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J. Neurosci. 30 (2010), 4408–4418.
198. Yarnall, A.J., Rochester, L., Baker, M.R., David, R., Khoo, T.K., Duncan, G.W., Galna, B., Burn, D.J., Short latency afferent inhibition: a biomarker for mild cognitive impairment in Parkinson's disease?. Mov. Disord. 28 (2013), 1285–1288.
199. Yi, F., Catudio-Garrett, E., Gábriel, R., Wilhelm, M., Erdelyi, F., Szabo, G., Deisseroth, K., Lawrence, J., Hippocampal “cholinergic interneurons” visualized with the choline acetyltransferase promoter: anatomical distribution, intrinsic membrane properties, neurochemical characteristics, and capacity for cholinergic modulation. Front. Synaptic Neurosci., 7, 2015, 4.
200. Zaborszky, L., Pang, K., Somogyi, J., Nadasdy, Z., Kallo, I., The basal forebrain corticopetal system revisited. Ann. N Y Acad. Sci. 877 (1999), 339–367.
201. Zaborszky, L., Hoemke, L., Mohlberg, H., Schleicher, A., Amunts, K., Zilles, K., Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain. Neuroimage 42 (2008), 1127–1141.
202. Zaborszky, L., Csordas, A., Mosca, K., Kim, J., Gielow, M.R., Vadasz, C., Nadasdy, Z., Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb. Cortex 25 (2015), 118–137.
203. th Edition, 2015, Elsevier, 491–507.
204. Zhang, X., Ge, X.Y., Wang, J.G., Wang, Y.L., Wang, Y., Yu, Y., Li, P.P., Lu, C.B., Induction of long-term oscillations in the γ frequency band by nAChR activation in rat hippocampal CA3 area. Neuroscience 301 (2015), 49–60.
205. Zhao, Y., Marín, O., Hermesz, E., Powell, A., Flames, N., Palkovits, M., Rubenstein, J.L., Westphal, H., The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl. Acad. Sci. USA 100 (2003), 9005–9010.
206. Zhong, C., Du, C., Hancock, M., Mertz, M., Talmage, D.A., Role, L.W., Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of alpha7 nicotinic acetylcholine receptors. J. Neurosci. 28 (2008), 9111–9116.
207. Zhong, C., Talmage, D.A., Role, L.W., Nicotine elicits prolonged calcium signaling along ventral hippocampal axons. PLoS ONE, 8, 2013, e82719.
208. Ziegler, D.A., Wonderlick, J.S., Ashourian, P., Hansen, L.A., Young, J.C., Murphy, A.J., Koppuzha, C.K., Growdon, J.H., Corkin, S., Substantia nigra volume loss before basal forebrain degeneration in early Parkinson disease. JAMA Neurol. 70 (2013), 241–247.
209. Zurkovsky, L., Bychkov, E., Tsakem, E.L., Siedlecki, C., Blakely, R.D., Gurevich, E.V., Cognitive effects of dopamine depletion in the context of diminished acetylcholine signaling capacity in mice. Dis. Model. Mech. 6 (2013), 171–183.