Basal forebrain cholinergic modulation of sleep transitions

Sleep

Volumn 37, Issue 12, 2014, Pages 1941-1951

  Ozen Irmak, Simal ^a   De Lecea, Luis ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b MSLS Bld   (United States)

Author keywords

Choline acetyltransferase (ChAT); Electroencephalogram (EEG); Horizontal limb of diagonal band (HLDB); Nucleus basalis (NB); Optogenetics; Recordings from freely moving animals; REM sleep; Slow wave sleep (NREM); Substantia innominata (SI); Transgenic mice

Indexed keywords

CRE RECOMBINASE;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; CHOLINERGIC NERVE CELL; CHOLINERGIC STIMULATION; CONTROLLED STUDY; DROWSINESS; ELECTROENCEPHALOGRAM; FOREBRAIN; GLOBUS PALLIDUS; LATENT PERIOD; MALE; MOUSE; NEOCORTEX; NEUROMODULATION; NONHUMAN; NONREM SLEEP; OPTOGENETICS; PHOTOSTIMULATION; REM SLEEP; SLEEP; SLEEP PATTERN; STRIA TERMINALIS; SUBSTANTIA INNOMINATA; TIME; VENTRAL PALLIDUM; VIRAL GENE DELIVERY SYSTEM; WAKEFULNESS; ANIMAL; C57BL MOUSE; CYTOLOGY; ELECTROENCEPHALOGRAPHY; METABOLISM; PHYSIOLOGY;

ANIMALS; AROUSAL; BASAL FOREBRAIN; CHOLINERGIC NEURONS; ELECTROENCEPHALOGRAPHY; MALE; MICE; MICE, INBRED C57BL; OPTOGENETICS; SLEEP; SLEEP, REM; SUBSTANTIA INNOMINATA; WAKEFULNESS;

EID: 84914128656     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.4246     Document Type: Article

References (57)

1. Whitehouse PJ, Price DL, Clark AW, Coyle JT, DeLong MR. Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 1981;10:122-6.
2. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 1982;215:1237-9.
3. Damasio AR, Graff-Radford NR, Eslinger PJ, Damasio H, Kassell N. Amnesia following basal forebrain lesions. Arch Neurol 1985;42:263-71.
4. Zaborszky L, van del Pol A, Gyengesi E. The basal forebrain cholinergic system in mice. In: Watson C, Paxinos G, Puelle L, eds. The Mouse Nervous System. Elsevier, 2011:680-92.
5. Buzsaki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 1988;8:4007-26.
6. Jimenez-Capdeville ME, Dykes RW, Myasnikov AA. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences. J Comp Neurol 1997;381:53-67.
7. Cape EG, Jones BE. Effects of glutamate agonist versus procaine microinjections into the basal forebrain cholinergic cell area upon gamma and theta EEG activity and sleep-wake state. Eur J Neurosci 2000;12:2166-84.
8. Cape EG, Manns ID, Alonso A, Beaudet A, Jones BE. Neurotensininduced bursting of cholinergic basal forebrain neurons promotes gamma and theta cortical activity together with waking and paradoxical sleep. J Neurosci 2000;20:8452-61.
9. Detari L. Tonic and phasic influence of basal forebrain unit activity on the cortical EEG. Behav Brain Res 2000;115:159-70.
10. Albanese A, Gozzo S, Iacopino C, Altavista MC. Strain-dependent variations in the number of forebrain cholinergic neurons. Brain Res 1985;334:380-4.
11. Kalesnykas G, Puolivali J, Sirvio J, Miettinen R. Cholinergic neurons in the basal forebrain of aged female mice. Brain Res 2004;1022:148-56.
12. Perez SE, Dar S, Ikonomovic MD, DeKosky ST, Mufson EJ. Cholinergic forebrain degeneration in the APPswe/PS1DeltaE9 transgenic mouse. Neurobiol Dis 2007;28:3-15.
13. Gritti I, Henny P, Galloni F, Mainville L, Mariotti M, Jones BE. 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 2006;143:1051-64.
14. Zaborszky L, Pang K, Somogyi J, Nadasdy Z, Kallo I. The basal forebrain corticopetal system revisited. Ann N Y Acad Sci 1999;877:339-67.
15. Zaborszky L, Buhl DL, Pobalashingham S, Bjaalie JG, Nadasdy Z. Three-dimensional chemoarchitecture of the basal forebrain: spatially specific association of cholinergic and calcium binding protein-containing neurons. Neuroscience 2005;136:697-713.
16. Castaneda MT, Sanabria ER, Hernandez S, et al. Glutamic acid decarboxylase isoforms are differentially distributed in the septal region of the rat. Neurosci Res 2005;52:107-19.
17. Nadasdy Z, Varsanyi P, Zaborszky L. Clustering of large cell populations: method and application to the basal forebrain cholinergic system. J Neurosci Methods 2010;194:46-55.
18. Lee MG, Manns ID, Alonso A, Jones BE. Sleep-wake related discharge properties of basal forebrain neurons recorded with micropipettes in head-fixed rats. J Neurophysiol 2004;92:1182-98.
19. Lee MG, Hassani OK, Alonso A, Jones BE. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 2005;25:4365-9.
20. Hassani OK, Lee MG, Henny P, Jones BE. Discharge profiles of identified GABAergic in comparison to cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. J Neurosci 2009;29:11828-40.
21. Takahashi K, Lin JS, Sakai K. Characterization and mapping of sleepwaking specific neurons in the basal forebrain and preoptic hypothalamus in mice. Neuroscience 2009;161:269-92.
22. Manns ID, Alonso A, Jones BE. Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 2000;20:1505-18.
23. Duque A, Balatoni B, Detari L, Zaborszky L. EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 2000;84:1627-35.
24. Manns ID, Alonso A, Jones BE. Discharge profiles of juxtacellularly labeled and immunohistochemically identified GABAergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 2000;20:9252-63.
25. Metherate R, Ashe JH. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res 1991;559:163-7.
26. Metherate R, Ashe JH. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 1993;14:132-43.
27. Metherate R, Cox CL, Ashe JH. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 1992;12:4701-11.
28. Nagel G, Szellas T, Huhn W, et al. Channelrhodopsin-2, a directly lightgated cation-selective membrane channel. Proc Natl Acad Sci U S A 2003;100:13940-5.
29. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecondtimescale, genetically targeted optical control of neural activity. Nat Neurosci 2005;8:1263-8.
30. Zhang F, Wang LP, Boyden ES, Deisseroth K. Channelrhodopsin-2 and optical control of excitable cells. Nat Methods 2006;3:785-92.
31. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007;450:420-4.
32. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009;459:698-702.
33. Carter ME, Yizhar O, Chikahisa S, et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci 2010;13:1526-33.
34. Rolls A, Colas D, Adamantidis A, et al. Optogenetic disruption of sleep continuity impairs memory consolidation. Proc Natl Acad Sci U S A 2011;108:13305-10.
35. Lowell BB, Olson D, Yu J. Development and phenotype of ChAT-IRES-Cre mice. MGI Direct Data Submission, 2006.
36. English DF, Ibanez-Sandoval O, Stark E, et al. GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 2011;15:123-30.
37. Benington JH, Kodali SK, Heller HC. Scoring transitions to REM sleep in rats based on the EEG phenomena of pre-REM sleep: an improved analysis of sleep structure. Sleep 1994;17:28-36.
38. Witten IB, Lin SC, Brodsky M, et al. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 2010;330:1677-81.
39. Unal CT, Golowasch JP, Zaborszky L. Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front Behav Neurosci 2012;6:21.
40. Carter ME, Adamantidis A, Ohtsu H, Deisseroth K, de Lecea L. Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions. J Neurosci 2009;29:10939-49.
41. Han Y, Shi YF, Xi W, et al. Selective activation of cholinergic basal forebrain neurons induces immediate sleep-wake transitions. Curr Biol 2014;24:693-8.
42. Khateb A, Muhlethaler M, Alonso A, Serafin M, Mainville L, Jones BE. Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes. Neuroscience 1992;51:489-94.
43. Woolf NJ, Butcher LL. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 1986;16:603-37.
44. Hallanger AE, Wainer BH. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 1988;274:483-515.
45. Semba K, Reiner PB, McGeer EG, Fibiger HC. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 1988;267:433-53.
46. Jones BE, Cuello AC. Afferents to the basal forebrain cholinergic cell area from pontomesencephalic-catecholamine, serotonin, and acetylcholine-neurons. Neuroscience 1989;31:37-61.
47. Losier BJ, Semba K. Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res 1993;604:41-52.
48. Ren J, Qin C, Hu F, et al. Habenula "cholinergic" neurons co-release glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 2011;69:445-52.
49. Zhao S, Ting JT, Atallah HE, et al. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat Methods 2011;8:745-52.
50. Yang C, McKenna JT, Zant JC, Winston S, Basheer R, Brown RE. Cholinergic neurons excite cortically projecting basal forebrain GABAergic neurons. J Neurosci 2014;34:2832-44.
51. Kolisnyk B, Guzman MS, Raulic S, et al. ChAT-ChR2-EYFP mice have enhanced motor endurance but show deficits in attention and several additional cognitive domains. J Neurosci 2013;33:10427-38.
52. Carter ME, Brill J, Bonnavion P, Huguenard JR, Huerta R, de Lecea L. Mechanism for hypocretin-mediated sleep-to-wake transitions. Proc Natl Acad Sci U S A 2012;109:E2635-44.
53. de Lecea L, Carter ME, Adamantidis A. Shining light on wakefulness and arousal. Biol Psychiatry 2012;71:1046-52.
54. Zaborszky L, Heimer L, Eckenstein F, Leranth C. GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J Comp Neurol 1986;250:282-95.
55. Zaborszky L, Duque A. Local synaptic connections of basal forebrain neurons. Behav Brain Res 2000;115:143-58.
56. Freund TF, Meskenaite V. aγ-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc Natl Acad Sci U S A 1992;89:738-42.
57. Lein ES, Hawrylycz MJ, Ao N, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007;445:168-76.