Illuminating the role of cholinergic signaling in circuits of attention and emotionally salient behaviors

Frontiers in Synaptic Neuroscience

Volumn 6, Issue OCT, 2014, Pages

  Luchicchi, Antonio ^a   Bloem, Bernard ^a,b   Viaña, John Noel M ^a   Mansvelder, Huibert D ^a   Role, Lorna W ^c  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c State University of New York at Stony Brook   (United States)

Author keywords

Acetylcholine; Attention; Limbic circuitries; Nicotinic receptors; Optogenetics

Indexed keywords

ACETYLCHOLINE; NEUROTRANSMITTER; OPSIN;

AMYGDALOID NUCLEUS; ATTENTION; AUDITORY CORTEX; BEHAVIOR; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; COGNITION; CORPUS STRIATUM; DOPAMINE RELEASE; EMOTION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXECUTIVE FUNCTION; FOLLOW UP; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERNEURON; LEARNING; LOCOMOTION; MEMORY; MOTIVATION; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OPTOGENETICS; PREFRONTAL CORTEX; PYRAMIDAL NERVE CELL; REVIEW; REWARD; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84910008357     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2014.00024     Document Type: Review

References (118)

1. Alitto, H. J., and Dan, Y. (2013). Cell-type-specific modulation of neocortical activity by basal forebrain input. Front. Syst. Neurosci. 6:79. doi: 10.3389/fnsys.2012.00079
2. Arroyo, S., Bennett, C., Aziz, D., Brown, S. P., and Hestrin, S. (2012). Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons. J. Neurosci. 32, 3859-3864. doi: 10.1523/JNEUROSCI.0115-12.2012
3. Arroyo, S., Bennett, C., and Hestrin, S. (2014). Nicotinic modulation of cortical circuits. Front. Neural Circuits 8:30. doi: 10.3389/fncir.2014.00030
4. Atasoy, D., Aponte, Y., Su, H. H., and Sternson, S. M. (2008). A FLEX switch targets channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025-7030. doi: 10.1523/jneurosci.1954-08.2008
5. Bell, L. A., Bell, K. A., and McQuiston, A. R. (2013). Synaptic muscarinic response types in hippocampal CA1 interneurons depend on different levels of presynaptic activity and different muscarinic receptor subtypes. Neuropharmacology 73, 160-173. doi: 10.1016/j.neuropharm.2013.05.026
6. Bell, K. A., Shim, H., Chen, C. K., and McQuiston, A. R. (2011). Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain α4 and Β2 subunits. Neuropharmacology 61, 1379-1388. doi: 10.1016/j.neuropharm.2011.08.024
7. Bennett, C., Arroyo, S., Berns, D., and Hestrin, S. (2012). Mechanisms generating dual-component nicotinic EPSCs in cortical interneurons. J. Neurosci. 32, 17287-17296. doi: 10.1523/jneurosci.3565-12.2012
8. Bloem, B., Poorthuis, R. B., and Mansvelder, H. D. (2014). Cholinergic modulation of the medial prefrontal cortex: the role of nicotinic receptors in attention and regulation of neuronal activity. Front. Neural Circuits 8:17. doi: 10.3389/fncir.2014.00017
9. Blokland, A., Honig, W., and Raaijmakers, W. G. M. (1992). Effects of intra-hippocampal scopolamine injections in a repeated spatial acquisition task in the rat. Psychopharmacology (Berl) 109, 373-376. doi: 10.1007/bf02245886
10. Briggs, F., Mangun, G. R., and Usrey, W. M. (2013). Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits. Nature 499, 476-480. doi: 10.1038/nature12276
11. Brown, C. E., Sweetnam, D., Beange, M., Nahirney, P. C., and Nashmi, R. (2012a). α4* nicotinic acetylcholine receptors modulate experience-based cortical depression in the adult mouse somatosensory cortex. J. Neurosci. 32, 1207-1219. doi: 10.1523/JNEUROSCI.4568-11.2012
12. Brown, M. T. C., Tan, K. R., O'Connor, E. C., Nikonenko, I., Muller, D., and Lüscher, C. (2012b). Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 492, 452-456. doi: 10.1038/nature11657
13. Cachope, R., and Cheer, J. F. (2014). Local control of striatal dopamine release. Front. Behav. Neurosci. 8:188. doi: 10.3389/fnbeh.2014.00188
14. Cachope, R., Mateo, Y., Mathur, B. N., Irving, J., Wang, H. L., Morales, M., et al. (2012). Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2, 33-41. doi: 10.1016/j.celrep.2012.05.011
15. Champtiaux, N., Kalivas, P. W., and Bardo, M. T. (2006). Contribution of dihydro-beta-erythroidine sensitive nicotinic acetylcholine receptors in the ventral tegmental area to cocaine-induced behavioral sensitization in rats. Behav. Brain Res. 168, 120-126. doi: 10.1016/j.bbr.2005.10.017
16. Changeux, J.-P. (2010). Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat. Rev. Neurosci. 11, 389-401. doi: 10.1038/nrn2849
17. Christophe, E., Roebuck, A., Staiger, J. F., Lavery, D. J., Charpak, S., and Audinat, E. (2002). Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J. Neurophysiol. 88, 1318-1327. doi: 10.1152/jn.00199.2002
18. Constantinople, C. M., and Bruno, R. M. (2013). Deep cortical layers are activated directly by thalamus. Science 340, 1591-1594. doi: 10.1126/science.1236425
19. Corrigall, W. A., Coen, K. M., Zhang, J., and Adamson, L. K. (2002). Pharmacological manipulations of the pedunculopontine tegmental nucleus in the rat reduce self-administration of both nicotine and cocaine. Psychopharmacology (Berl) 160, 198-205. doi: 10.1007/s00213-001-0965-2
20. Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., et al. (2007). Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54, 73-87. doi: 10.1016/j.neuron.2007.03.006
21. Court, J., Martin-Ruiz, C., Piggott, M., Spurden, D., Griffiths, M., and Perry, E. (2001). Nicotinic receptor abnormalities in Alzheimer's disease. Biol. Psychiatry 49, 175-184. doi: 10.1016/s0006-3223(00)01116-1
22. Cruikshank, S. J., Ahmed, O. J., Stevens, T. R., Patrick, S. L., Gonzalez, A. N., Elmaleh, M., et al. (2012). Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813-17823. doi: 10.1523/JNEUROSCI.3231-12.2012
23. Dani, J. A., and Harris, R. A. (2005). Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat. Neurosci. 8, 1465-1470. doi: 10.1038/nn1580
24. Dautan, D., Huerta-Ocampo, I., Witten, I. B., Deisseroth, K., Bolam, J. P., Gerdjikov, T., et al. (2014). A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J. Neurosci. 34, 4509-4518. doi: 10.1523/jneurosci.5071-13.2014
25. Deco, G., and Thiele, A. (2011). Cholinergic control of cortical network interactions enables feedback-mediated attentional modulation. Eur. J. Neurosci. 34, 146-157. doi: 10.1111/j.1460-9568.2011.07749.x
26. Deisseroth, K. (2011). Optogenetics. Nat. Methods 8, 26-29. doi: 10.1038/nmeth.f.324
27. Descarries, L., Gisiger, V., and Steriade, M. (1997). Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol. 53, 603-625. doi: 10.1016/s0301-0082(97)00050-6
28. Disney, A. A., Aoki, C., and Hawken, M. J. (2007). Gain modulation by nicotine in macaque V1. Neuron 56, 701-713. doi: 10.1016/j.neuron.2007.09.034
29. Disney, A. A., Aoki, C., and Hawken, M. J. (2012). Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. J. Neurophysiol. 108, 1907-1923. doi: 10.1152/jn.00188.2012
30. Douglas, R. J., and Martin, K. A. C. (2004). Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419-451. doi: 10.1146/annurev.neuro.27.070203.144152
31. Duque, A., Balatoni, B., Detari, L., and Zaborszky, L. (2000). EEG correlation of the discharge properties of identified neurons in the basal forebrain. J. Neurophysiol. 84, 1627-1635.
32. Dutar, P., Bassant, M. H., Senut, M. C., and Lamour, Y. (1995). The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 75, 393-427.
33. Exley, R., and Cragg, S. J. (2008). Presynaptic nicotinic receptors: a dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br. J. Pharmacol. 153(Suppl. 1), S283-S297. doi: 10.1038/sj.bjp.0707510
34. Frotscher, M., and Léránth, C. (1985). Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 239, 237-246. doi: 10.1002/cne.902390210
35. Galarraga, E., Hernández-López, S., Reyes, A., Miranda, I., Bermudez-Rattoni, F., Vilchis, C., et al. (1999). Cholinergic modulation of neostriatal output: a functional antagonism between different types of muscarinic receptors. J. Neurosci. 19, 3629-3638.
36. Gittis, A. H., Nelson, A. B., Thwin, M. T., Palop, J. J., and Kreitzer, A. C. (2010). Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J. Neurosci. 30, 2223-2234. doi: 10.1523/jneurosci.4870-09.2010
37. Goard, M., and Dan, Y. (2009). Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12, 1444-1449. doi: 10.1038/nn.2402
38. Gotti, C., and Clementi, F. (2004). Neuronal nicotinic receptors: from structure to pathology. Prog. Neurobiol. 74, 363-396. doi: 10.1016/j.pneurobio.2004.09.006
39. Gras, C., Amilhon, B., Lepicard, E. M., Poirel, O., Vinatier, J., Herbin, M., et al. (2008). The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat. Neurosci. 11, 292-300. doi: 10.1038/nn2052
40. Griguoli, M., and Cherubini, E. (2012). Regulation of hippocampal inhibitory circuits by nicotinic acetylcholine receptors. J. Physiol. 590, 655-666. doi: 10.1113/jphysiol.2011.220095
41. Gu, Z., and Yakel, J. L. (2011). Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71, 155-165. doi: 10.1016/j.neuron.2011.04.026
42. Gulledge, A. T., Bucci, D. J., Zhang, S. S., Matsui, M., and Yeh, H. H. (2009). M1 receptors mediate cholinergic modulation of excitability in neocortical pyramidal neurons. J. Neurosci. 29, 9888-9902. doi: 10.1523/jneurosci.1366-09.2009
43. Gulledge, A. T., Park, S. B., Kawaguchi, Y., and Stuart, G. J. (2007). Heterogeneity of phasic cholinergic signaling in neocortical neurons. J. Neurophysiol. 97, 2215-2229. doi: 10.1152/jn.00493.2006
44. Hasselmo, M. E., and Giocomo, L. M. (2006). Cholinergic modulation of cortical function. J. Mol. Neurosci. 30, 133-136. doi: 10.1385/JMN:30:1:133
45. Hasselmo, M. E., and Sarter, M. (2011). Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36, 52-73. doi: 10.1038/npp.2010.104
46. Higley, M. J., Gittis, A. H., Oldenburg, I. A., Balthasar, N., Seal, R. P., Edwards, R. H., et al. (2011). Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum. PLoS One 6:e19155. doi: 10.1371/journal.pone.0019155
47. Howe, W. M., Berry, A. S., Francois, J., Gilmour, G., Carp, J. M., Tricklebank, M., et al. (2013). 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, 8742-8752. doi: 10.1523/jneurosci.5809-12.2013
48. Huang, Z. J., and Zeng, H. (2013). Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36, 183-215. doi: 10.1146/annurev-neuro-062012-170307
49. Jiang, L., López-Hernández, G. Y., Lederman, J., Talmage, D. A., and Role, W. L. (2014). Optogenetic studies of nicotinic contributions to cholinergic signaling in the central nervous system. Rev. Neurosci. doi: 10.1515/revneuro-2014-0032. [Epub ahead of print].
50. Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., and Zhu, J. J. (2013). The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210-218. doi: 10.1038/nn.3305
51. Joshua, M., Adler, A., Mitelman, R., Vaadia, E., and Bergman, H. (2008). Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J. Neurosci. 28, 11673-11684. doi: 10.1523/jneurosci.3839-08.2008
52. Kalmbach, A., Hedrick, T., and Waters, J. (2012). Selective optogenetic stimulation of cholinergic axons in neocortex. J. Neurophysiol. 107, 2008-2019. doi: 10.1152/jn.00870.2011
53. Kassam, S. M., Herman, P. M., Goodfellow, N. M., Alves, N. C., and Lambe, E. K. (2008). Developmental excitation of corticothalamic neurons by nicotinic acetylcholine receptors. J. Neurosci. 28, 8756-8764. doi: 10.1523/JNEUROSCI.2645-08.2008
54. Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E. S., Mackie, K., et al. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19, 4544-4558.
55. Kawai, H., Lazar, R., and Metherate, R. (2007). Nicotinic control of axon excitability regulates thalamocortical transmission. Nat. Neurosci. 10, 1168-1175. doi: 10.1038/nn1956
56. Kilgard, M. P., and Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714-1718. doi: 10.1126/science.279.5357.1714
57. Kimura, F., and Baughman, R. W. (1997). Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J. Neurophysiol. 77, 709-716.
58. Kimura, F., Fukuda, M., and Tsumoto, T. (1999). Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input. Eur. J. Neurosci. 11, 3597-3609. doi: 10.1046/j.1460-9568.1999.00779.x
59. Kimura, R., Safari, M.-S., Mirnajafi-Zadeh, J., Kimura, R., Ebina, T., Yanagawa, Y., et al. (2014). Curtailing effect of awakening on visual responses of cortical neurons by cholinergic activation of inhibitory circuits. J. Neurosci. 34, 10122-10133. doi: 10.1523/jneurosci.0863-14.2014
60. Klinkenberg, I., Sambeth, A., and Blokland, A. (2011). Acetylcholine and attention. Behav. Brain Res. 221, 430-442. doi: 10.1016/j.bbr.2010.11.033
61. Koós, T., and Tepper, J. M. (1999). Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 2, 467-472. doi: 10.1038/8138
62. Koós, T., and Tepper, J. M. (2002). Dual cholinergic control of fast-spiking interneurons in the neostriatum. J. Neurosci. 22, 529-535.
63. Lambe, E. K., Picciotto, M. R., and Aghajanian, G. K. (2003). Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28, 216-225. doi: 10.1038/sj.npp.1300032
64. Leão, R. N., Mikulovic, S., Leão, K. E., Munguba, H., Gezelius, H., Enjin, A., et al. (2012). OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat. Neurosci. 15, 1524-1530. doi: 10.1038/nn.3235
65. Leslie, F. M., Mojica, C. Y., and Reynaga, D. D. (2013). Nicotinic receptors in addiction pathways. Mol. Pharmacol. 83, 753-758. doi: 10.1124/mol.112.083659
66. Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., et al. (2011). A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335. doi: 10.1038/nature10674
67. Levin, E. D., Bradley, A., Addy, N., and Sigurani, N. (2002). Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory. Neuroscience 109, 757-765. doi: 10.1016/s0306-4522(01)00538-3
68. Mann, E. O., Suckling, J. M., Hajos, N., Greenfield, S. A., and Paulsen, O. (2005). Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45, 105-117. doi: 10.1016/j.neuron.2004.12.016
69. Manns, I. D., Alonso, A., and Jones, B. E. (2000). Discharge profiles of juxtacellularly labeled and immunohistochemically identified GABAergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci. 20, 9252-9263.
70. Martin, L. F., and Freedman, R. (2007). Schizophrenia and the alpha7 nicotinic acetylcholine receptor. Int. Rev. Neurobiol. 78, 225-246. doi: 10.1016/S0074-7742(06)78008-4
71. Mesulam, M. M. (1995). Cholinergic pathways and the ascending reticular activating system of the human brain. Ann. N Y Acad. Sci. 757, 169-179. doi: 10.1111/j.1749-6632.1995.tb17472.x
72. Metherate, R., Cox, C. L., and Ashe, J. H. (1992). Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701-4711.
73. Morris, G., Arkadir, D., Nevet, A., Vaadia, E., and Bergman, H. (2004). Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43, 133-143. doi: 10.1016/j.neuron.2004.06.012
74. Nagode, D. A., Tang, A. H., Karson, M. A., Klugmann, M., and Alger, B. E. (2011). Optogenetic release of ACh induces rhythmic bursts of perisomatic IPSCs in hippocampus. PLoS One 6:e27691. doi: 10.1371/journal.pone.0027691
75. Nagode, D. A., Tang, A.-H., Yang, K., and Alger, B. E. (2014). Optogenetic identification of an intrinsic cholinergically driven inhibitory oscillator sensitive to cannabinoids and opioids in hippocampal CA1. J. Physiol. 592, 103-123. doi: 10.1113/jphysiol.2013.257428
76. Nelson, A. B., Hammack, N., Yang, C. F., Shah, N. M., Seal, R. P., and Kreitzer, A. C. (2014). Striatal cholinergic interneurons drive GABA release from dopamine terminals. Neuron 82, 63-70. doi: 10.1016/j.neuron.2014.01.023
77. Oldford, E., and Castro-Alamancos, M. A. (2003). Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the "barrel cortex" in vivo. Neuroscience 117, 769-778. doi: 10.1016/s0306-4522(02)00663-2
78. Paez-Gonzalez, P., Asrican, B., Rodriguez, E., and Kuo, C. T. (2014). Identification of distinct ChAT(+) neurons and activity-dependent control of postnatal SVZ neurogenesis. Nat. Neurosci. 17, 934-942. doi: 10.1038/nn.3734
79. Parikh, V., Kozak, R., Martinez, V., and Sarter, M. (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56, 141-154. doi: 10.1016/j.neuron.2007.08.025
80. Parikh, V., and Sarter, M. (2008). Cholinergic mediation of attention. Ann. N Y Acad. Sci. 1129, 225-235. doi: 10.1196/annals.1417.021
81. Passetti, F., Dalley, J. W., O'Connell, M. T., Everitt, B. J., and Robbins, T. W. (2000). Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur. J. Neurosci. 12, 3051-3058. doi: 10.1046/j.1460-9568.2000.00183.x
82. Picciotto, M. R., Higley, M. J., and Mineur, Y. S. (2012). Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76, 116-129. doi: 10.1016/j.neuron.2012.08.036
83. Pinto, L., Goard, M. J., Estandian, D., Xu, M., Kwan, A. C., Lee, S.-H., et al. (2013). Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16, 1857-1863. doi: 10.1038/nn.3552
84. Poorthuis, R. B., Bloem, B., Schak, B., Wester, J., de Kock, C. P. J., and Mansvelder, H. D. (2013). Layer-specific modulation of the prefrontal cortex by nicotinic acetylcholine receptors. Cereb. Cortex 23, 148-161. doi: 10.1093/cercor/bhr390
85. Poorthuis, R. B., Enke, L., and Letzkus, J. J. (2014). Cholinergic circuit modulation through differential recruitment of neocortical interneuron types during behaviour. J. Physiol. 592, 4155-4164. doi: 10.1113/jphysiol.2014.273862
86. Ren, J., Qin, C., Hu, F., Tan, J., Qiu, L., Zhao, S., et al. (2011). Habenula "cholinergic" neurons corelease glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69, 445-452. doi: 10.1016/j.neuron.2010.12.038
87. Rice, M. E., and Cragg, S. J. (2004). Nicotine amplifies reward-related dopamine signals in striatum. Nat. Neurosci. 7, 583-584. doi: 10.1038/nn1244
88. Roberts, M. J., Zinke, W., Guo, K., Robertson, R., McDonald, J. S., and Thiele, A. (2005). Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol. 93, 2062-2072. doi: 10.1152/jn.00911.2004
89. Role, L. W. (2014). "Cholinergic modulation of cortical-amygdala circuits and behavior. ABS S25," in Nicotinic Acetylcholine Receptors, Wellcome Trust Scientific Conference, eds I. Bermudez, N. Millar and S. Wonnacott.
90. Sarter, M., Lustig, C., Howe, W. M., Gritton, H., and Berry, A. S. (2014). Deterministic functions of cortical acetylcholine. Eur. J. Neurosci. 39, 1912-1920. doi: 10.1111/ejn.12515
91. Sarter, M., Parikh, V., and Howe, W. M. (2009). Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat. Rev. Neurosci. 10, 383-390. doi: 10.1038/nrn2635
92. Silver, M. A., Shenhav, A., and D'Esposito, M. (2008). Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron 60, 904-914. doi: 10.1016/j.neuron.2008.09.038
93. Smiley, J. F., Morrell, F., and Mesulam, M. M. (1997). Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp. Neurol. 144, 361-368. doi: 10.1006/exnr.1997.6413
94. Soma, S., Shimegi, S., Osaki, H., and Sato, H. (2012). Cholinergic modulation of response gain in the primary visual cortex of the macaque. J. Neurophysiol. 107, 283-291. doi: 10.1152/jn.00330.2011
95. Soma, S., Shimegi, S., Suematsu, N., Tamura, H., and Sato, H. (2013). Modulation-specific and laminar-dependent effects of acetylcholine on visual responses in the rat primary visual cortex. PLoS One 8:e68430. doi: 10.1371/journal.pone.0068430
96. Straub, C., Tritsch, N. X., Hagan, N. A., Gu, C., and Sabatini, B. L. (2014). Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents. J. Neurosci. 34, 8557-8569. doi: 10.1523/jneurosci.0589-14.2014
97. Sun, Y.-G., Pita-Almenar, J. D., Wu, C.-S., Renger, J. J., Uebele, V. N., Lu, H.-C., et al. (2013). Biphasic cholinergic synaptic transmission controls action potential activity in thalamic reticular nucleus neurons. J. Neurosci. 33, 2048-2059. doi: 10.1523/JNEUROSCI.3177-12.2013
98. Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouèbe, G., et al. (2012). GABA neurons of the VTA drive conditioned place aversion. Neuron 73, 1173-1183. doi: 10.1016/j.neuron.2012.02.015
99. Thiele, A., Herrero, J. L., Distler, C., and Hoffmann, K.-P. (2012). Contribution of cholinergic and GABAergic mechanisms to direction tuning, discriminability, response reliability and neuronal rate correlations in macaque middle temporal area. J. Neurosci. 32, 16602-16615. doi: 10.1523/jneurosci.0554-12.2012
100. Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., and Cragg, S. J. (2012). Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64. doi: 10.1016/j.neuron.2012.04.038
101. Tu, B., Gu, Z., Shen, J.-X., Lamb, P. W., and Yakel, J. L. (2009). Characterization of a nicotine-sensitive neuronal population in rat entorhinal cortex. J. Neurosci. 29, 10436-10448. doi: 10.1523/jneurosci.2580-09.2009
102. Turrini, P., Casu, M. A., Wong, T. P., De Koninck, Y., Ribeiro-da-Silva, A., and Cuello, A. C. (2001). Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy. Neuroscience 105, 277-285. doi: 10.1016/s0306-4522(01)00172-5
103. Uhlhaas, P. J., Haenschel, C., Nikolić, D., and Singer, W. (2008). The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr. Bull. 34, 927-943. doi: 10.1093/schbul/sbn062
104. Uylings, H. B. M., Groenewegen, H. J., and Kolb, B. (2003). Do rats have a prefrontal cortex? Behav. Brain Res. 146, 3-17. doi: 10.1016/j.bbr.2003.09.028
105. Van Bockstaele, E. J., and Pickel, V. M. (1995). GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res. 682, 215-221. doi: 10.1016/0006-8993(95)00334-m
106. Van Zessen, R., Phillips, J. L., Budygin, E. A., and Stuber, G. D. (2012). Activation of VTA GABA neurons disrupts reward consumption. Neuron 73, 1184-1194. doi: 10.1016/j.neuron.2012.02.016
107. von Engelhardt, J., Eliava, M., Meyer, A. H., Rozov, A., and Monyer, H. (2007). Functional characterization of intrinsic cholinergic interneurons in the cortex. J. Neurosci. 27, 5633-5642. doi: 10.1523/jneurosci.4647-06.2007
108. Wang, X.-J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90, 1195-1268. doi: 10.1152/physrev.00035.2008
109. Wang, L., Shang, S., Kang, X., Teng, S., Zhu, F., Liu, B., et al. (2014). Modulation of dopamine release in the striatum by physiologically relevant levels of nicotine. Nat. Commun. 5:3925. doi: 10.1038/ncomms4925
110. Wess, J. (2003). Novel insights into muscarinic acetylcholine receptor function using gene targeting technology. Trends Pharmacol. Sci. 24, 414-420. doi: 10.1016/s0165-6147(03)00195-0
111. Wilson, R. I., and Nicoll, R. A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592. doi: 10.1038/35069076
112. Witten, I. B., Lin, S.-C., Brodsky, M., Prakash, R., Diester, I., Anikeeva, P., et al. (2010). Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677-1681. doi: 10.1126/science.1193771
113. Witten, I. B., Steinberg, E. E., Lee, S. Y., Davidson, T. J., Zalocusky, K. A., Brodsky, M., et al. (2011). Recombinase-driver rat lines: tools, techniques and optogenetic application to dopamine-mediated reinforcement. Neuron 72, 721-733. doi: 10.1016/j.neuron.2011.10.028
114. Wonnacott, S. (1997). Presynaptic nicotinic ACh receptors. Trends Neurosci. 20, 92-98. doi: 10.1016/s0166-2236(96)10073-4
115. Woolf, N. J. (1991). Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37, 475-524. doi: 10.1016/0301-0082(91)90006-m
116. Yakel, J. L. (2012). Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. Nicotine Tob. Res. 14, 1249-1257. doi: 10.1093/ntr/nts091
117. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., and Deisseroth, K. (2011). Optogenetics in neural systems. Neuron 71, 9-34. doi: 10.1016/j.neuron.2011.06.004
118. Zaborszky, L., Pang, K., Somogyi, J., Nadasdy, Z., and Kallo, I. (1999). The basal forebrain corticopetal system revisited. Ann. N Y Acad. Sci. 877, 339-367. doi: 10.1111/j.1749-6632.1999.tb09276.x