A unifying computational framework for stability and flexibility of arousal

Frontiers in Systems Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Kosse, Christin ^a   Burdakov, Denis ^a,b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Arousal; Computation; Control; Histamine; Hypocretin; Hypothalamus; Narcolepsy; Orexin

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; HISTAMINE; NORADRENALIN; OREXIN; OREXIN 2 RECEPTOR;

AROUSAL; ARTICLE; BEHAVIOR; COMPUTER PREDICTION; COMPUTER SIMULATION; DOPAMINERGIC NERVE CELL; DYNAMICS; FEEDBACK SYSTEM; HUMAN; MATHEMATICAL COMPUTING; NARCOLEPSY; NERVE CELL; NERVE CELL NETWORK; NEUROPHYSIOLOGICAL MONITORING; NEUROTRANSMISSION; PROTEIN EXPRESSION; SEROTONINERGIC NERVE CELL; SIGNAL PROCESSING;

EID: 84908253463     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00192     Document Type: Article

References (74)

1. Achermann, P., and Borbély, A. A. (2003). Mathematical models of sleep regulation. Front. Biosci. 8, s683-s693. doi: 10.2741/1064
2. Adamantidis, A., Carter, M. C., and de Lecea, L. (2010). Optogenetic deconstruction of sleep-wake circuitry in the brain. Front. Mol. Neurosci. 2:31. doi: 10.3389/neuro.02.031.2009
3. Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K., and de Lecea, L. (2007). Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-424. doi: 10.1038/nature06310
4. Aponte, Y., Atasoy, D., and Sternson, S. M. (2011). AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat. Neurosci. 14, 351-355. doi: 10.1038/nn.2739
5. Armstrong, C., Krook-Magnuson, E., Oijala, M., and Soltesz, I. (2013). Closed-loop optogenetic intervention in mice. Nat. Protoc. 8, 1475-1493. doi: 10.1038/nprot.2013.080
6. Aston-Jones, G., and Bloom, F. E. (1981). Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J. Neurosci. 1, 887-900.
7. Aström, K., and Hagglund, T. (1995). PID Controllers Theory, Design and Tuning. Intrument Society of America.
8. Atasoy, D., Betley, J. N., Su, H. H., and Sternson, S. M. (2012). Deconstruction of a neural circuit for hunger. Nature 488, 172-177. doi: 10.1038/nature11270
9. Bayer, L., Eggermann, E., Serafin, M., Grivel, J., Machard, D., Muhlethaler, M., et al. (2005). Opposite effects of noradrenaline and acetylcholine upon hypocretin/orexin versus melanin concentrating hormone neurons in rat hypothalamic slices. Neuroscience 130, 807-811. doi: 10.1016/j.neuroscience.2004.10.032
10. Bhat, A., Shafi, F., and El Solh, A. A. (2008). Pharmacotherapy of insomnia. Expert Opin. Pharmacother. 9, 351-362. doi: 10.1517/14656566.9.3.351
11. Carter, M. E., Brill, J., Bonnavion, P., Huguenard, J. R., Huerta, R., and de Lecea, L. (2012). Mechanism for hypocretin-mediated sleep-to-wake transitions. Proc. Natl. Acad. Sci. U S A 109, E2635-E2644. doi: 10.1073/pnas.1202526109
12. Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., et al. (2010). Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526-1533. doi: 10.1038/nn.2682
13. Chemelli, R. M., Willie, J. T., Sinton, C. M., Elmquist, J. K., Scammell, T., Lee, C., et al. (1999). Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98, 437-451. doi: 10.1016/s0092-8674(00)81973-x
14. Csete, M. E., and Doyle, J. C. (2002). Reverse engineering of biological complexity. Science 295, 1664-1669. doi: 10.1126/science.1069981
15. Csete, M., and Doyle, J. (2004). Bow ties, metabolism and disease. Trends Biotechnol. 22, 446-450. doi: 10.1016/j.tibtech.2004.07.007
16. Dauvilliers, Y., Arnulf, I., and Mignot, E. (2007). Narcolepsy with cataplexy. Lancet 369, 499-511. doi: 10.1016/S0140-6736(07)60237-2
17. de Lecea, L., Jones, B. E., Boutrel, B., Borgland, S. L., Nishino, S., Bubser, M., et al. (2006). Addiction and arousal: alternative roles of hypothalamic peptides. J. Neurosci. 26, 10372-10375. doi: 10.1523/jneurosci.3118-06.2006
18. de Lecea, L., Kilduff, T. S., Peyron, C., Gao, X., Foye, P. E., Danielson, P. E., et al. (1998). The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U S A 95, 322-327. doi: 10.1073/pnas.95.1.322
19. DiStefano, J., Stubberud, A., and Williams, I. (2012). Feedback and Control Systems. New York: McGrawHill.
20. Doyle, J. C., and Csete, M. (2011). Architecture, constraints and behavior. Proc. Natl. Acad. Sci. U S A 108(Suppl. 3), 15624-15630. doi: 10.1073/pnas.1103557108
21. Dworak, M., McCarley, R. W., Kim, T., Kalinchuk, A. V., and Basheer, R. (2010). Sleep and brain energy levels: ATP changes during sleep. J. Neurosci. 30, 9007-9016. doi: 10.1523/JNEUROSCI.1423-10.2010
22. Famm, K., Litt, B., Tracey, K. J., Boyden, E. S., and Slaoui, M. (2013). Drug discovery: a jump-start for electroceuticals. Nature 496, 159-161. doi: 10.1038/496159a
23. Franklin, D. W., and Wolpert, D. M. (2011). Computational mechanisms of sensorimotor control. Neuron 72, 425-442. doi: 10.1016/j.neuron.2011.10.006
24. Fulcher, B. D., Phillips, A. J., Postnova, S., and Robinson, P. A. (2014). A physiologically based model of orexinergic stabilization of sleep and wake. PLoS One 9:e91982. doi: 10.1371/journal.pone.0091982
25. Grivel, J., Cvetkovic, V., Bayer, L., Machard, D., Tobler, I., Mühlethaler, M., et al. (2005). The wake-promoting hypocretin/orexin neurons change their response to noradrenaline after sleep deprivation. J. Neurosci. 25, 4127-4130. doi: 10.1523/jneurosci.0666-05.2005
26. Gropp, E., Shanabrough, M., Borok, E., Xu, A. W., Janoschek, R., Buch, T., et al. (2005). Agouti-related peptide-expressing neurons are mandatory for feeding. Nat. Neurosci. 8, 1289-1291. doi: 10.1038/nn1548
27. Haas, H. L., Sergeeva, O. A., and Selbach, O. (2008). Histamine in the nervous system. Physiol. Rev. 88, 1183-1241. doi: 10.1152/physrev.00043.2007
28. Hagan, J. J., Leslie, R. A., Patel, S., Evans, M. L., Wattam, T. A., Holmes, S., et al. (1999). Orexin a activates locus coeruleus cell firing and increases arousal in the rat. Proc. Natl. Acad. Sci. U S A 96, 10911-10916. doi: 10.1073/pnas.96.19.10911
29. Hara, J., Beuckmann, C. T., Nambu, T., Willie, J. T., Chemelli, R. M., Sinton, C. M., et al. (2001). Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia and obesity. Neuron 30, 345-354. doi: 10.1016/s0896-6273(01)00293-8
30. Horvath, T. L., Stachenfeld, N. S., and Diano, S. (2014). A temperature hypothesis of hypothalamus-driven obesity. Yale J. Biol. Med. 87, 149-158.
31. Jones, B. E. (2003). Arousal systems. Front. Biosci. 8, s438-s451. doi: 10.2741/1074
32. Krashes, M. J., Koda, S., Ye, C., Rogan, S. C., Adams, A. C., Cusher, D. S., et al. (2011). Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 121, 1424-1428. doi: 10.1172/JCI46229
33. Kuwaki, T. (2011). Orexin links emotional stress to autonomic functions. Auton. Neurosci. 161, 20-27. doi: 10.1016/j.autneu.2010.08.004
34. Lee, M. G., Hassani, O. K., and Jones, B. E. (2005). Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J. Neurosci. 25, 6716-6720. doi: 10.1523/jneurosci.1887-05.2005
35. Li, Y., Gao, X. B., Sakurai, T., and van den Pol, A. N. (2002). Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36, 1169-1181. doi: 10.1016/s0896-6273(02)01132-7
36. Li, Y., and van den Pol, A. N. (2006). Differential target-dependent actions of coexpressed inhibitory dynorphin and excitatory hypocretin/orexin neuropeptides. J. Neurosci. 26, 13037-13047. doi: 10.1523/jneurosci.3380-06.2006
37. Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., et al. (1999). The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98, 365-376. doi: 10.1016/s0092-8674(00)81965-0
38. Liu, R. J., van den Pol, A. N., and Aghajanian, G. K. (2002). Hypocretins (orexins) regulate serotonin neurons in the dorsal raphe nucleus by excitatory direct and inhibitory indirect actions. J. Neurosci. 22, 9453-9464.
39. Lu, J., Sherman, D., Devor, M., and Saper, C. B. (2006). A putative flip-flop switch for control of REM sleep. Nature 441, 589-594. doi: 10.1038/nature04767
40. Luquet, S., Perez, F. A., Hnasko, T. S., and Palmiter, R. D. (2005). NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310, 683-685. doi: 10.1126/science.1115524
41. Mieda, M., Hasegawa, E., Kisanuki, Y. Y., Sinton, C. M., Yanagisawa, M., and Sakurai, T. (2011). Differential roles of orexin receptor-1 and -2 in the regulation of non-REM and REM sleep. J. Neurosci. 31, 6518-6526. doi: 10.1523/JNEUROSCI.6506-10.2011
42. Mignot, E., Taheri, S., and Nishino, S. (2002). Sleeping with the hypothalamus: emerging therapeutic targets for sleep disorders. Nat. Neurosci. 5(Suppl.), 1071-1075. doi: 10.1038/nn944
43. Mileykovskiy, B. Y., Kiyashchenko, L. I., and Siegel, J. M. (2005). Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46, 787-798. doi: 10.1016/j.neuron.2005.04.035
44. Mochizuki, T., Arrigoni, E., Marcus, J. N., Clark, E. L., Yamamoto, M., Honer, M., et al. (2011). Orexin receptor 2 expression in the posterior hypothalamus rescues sleepiness in narcoleptic mice. Proc. Natl. Acad. Sci. U S A 108, 4471-4476. doi: 10.1073/pnas.1012456108
45. Muraki, Y., Yamanaka, A., Tsujino, N., Kilduff, T. S., Goto, K., and Sakurai, T. (2004). Serotonergic regulation of the orexin/hypocretin neurons through the 5-HT1A receptor. J. Neurosci. 24, 7159-7166. doi: 10.1523/jneurosci.1027-04.2004
46. Nishino, S., and Kanbayashi, T. (2005). Symptomatic narcolepsy, cataplexy and hypersomnia and their implications in the hypothalamic hypocretin/orexin system. Sleep Med. Rev. 9, 269-310. doi: 10.1016/j.smrv.2005.03.004
47. Nishino, S., Ripley, B., Overeem, S., Lammers, G. J., and Mignot, E. (2000). Hypocretin (orexin) deficiency in human narcolepsy. Lancet 355, 39-40. doi: 10.1016/s0140-6736(99)05582-8
48. Peyron, C., Faraco, J., Rogers, W., Ripley, B., Overeem, S., Charnay, Y., et al. (2000). A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat. Med. 6, 991-997. doi: 10.1038/79690
49. Peyron, C., Tighe, D. K., van den Pol, A. N., de lecea, L., Heller, H. C., Sutcliffe, J. G., et al. (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996-10015.
50. Sakurai, T. (2007). The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat. Rev. Neurosci. 8, 171-181. doi: 10.1038/nrn2092
51. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., et al. (1998). Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585. doi: 10.1016/s0092-8674(00)80949-6
52. Saper, C. B., Chou, T. C., and Scammell, T. E. (2001). The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 24, 726-731. doi: 10.1016/s0166-2236(00)02002-6
53. Saper, C. B., and Scammell, T. E. (2013). Emerging therapeutics in sleep. Ann. Neurol. 74, 435-440. doi: 10.1002/ana.24000
54. Schöne, C., Apergis-Schoute, J., Sakurai, T., Adamantidis, A., and Burdakov, D. (2014). Coreleased orexin and glutamate evoke nonredundant spike outputs and computations in histamine neurons. Cell Rep. 7, 697-704. doi: 10.1016/j.celrep.2014.03.055
55. Sohn, J. W., Elmquist, J. K., and Williams, K. W. (2013). Neuronal circuits that regulate feeding behavior and metabolism. Trends Neurosci. 36, 504-512. doi: 10.1016/j.tins.2013.05.003
56. Speakman, J. R., Levitsky, D. A., Allison, D. B., Bray, M. S., De Castro, J. M., Clegg, D. J., et al. (2011). Set points, settling points and some alternative models: theoretical options to understand how genes and environments combine to regulate body adiposity. Dis. Model. Mech. 4, 733-745. doi: 10.1242/dmm.008698
57. Takahashi, K., Lin, J. S., and Sakai, K. (2006). Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse. J. Neurosci. 26, 10292-10298. doi: 10.1523/jneurosci.2341-06.2006
58. Tecuapetla, F., Patel, J. C., Xenias, H., English, D., Tadros, I., Shah, F., et al. (2010). Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci. 30, 7105-7110. doi: 10.1523/JNEUROSCI.0265-10.2010
59. Thannickal, T. C., Moore, R. Y., Nienhuis, R., Ramanathan, L., Gulyani, S., Aldrich, M., et al. (2000). Reduced number of hypocretin neurons in human narcolepsy. Neuron 27, 469-474. doi: 10.1016/s0896-6273(00)00058-1
60. Tritsch, N. X., Ding, J. B., and Sabatini, B. L. (2012). Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490, 262-266. doi: 10.1038/nature11466
61. Uschakov, A., Grivel, J., Cvetkovic-Lopes, V., Bayer, L., Bernheim, L., Jones, B. E., et al. (2011). Sleep-deprivation regulates alpha-2 adrenergic responses of rat hypocretin/orexin neurons. PLoS One 6:e16672. doi: 10.1371/journal.pone.0016672
62. von Bertalanffy, L. (2013). General Systems Theory. New York: George Braziller.
63. Wiener, N. (1965). Cybernetics: Or Control and Communication in the Animal and the Machine. Cambridge, Massachusetts: The MIT Press.
64. Williams, R. H., Alexopoulos, H., Jensen, L. T., Fugger, L., and Burdakov, D. (2008). Adaptive sugar sensors in hypothalamic feeding circuits. Proc. Natl. Acad. Sci. U S A 105, 11975-11980. doi: 10.1073/pnas.0802687105
65. Williams, R. H., Jensen, L. T., Verkhratsky, A., Fugger, L., and Burdakov, D. (2007). Control of hypothalamic orexin neurons by acid and CO2. Proc. Natl. Acad. Sci. U S A 104, 10685-10690. doi: 10.1073/pnas.0702676104
66. Williams, R. H., Morton, A. J., and Burdakov, D. (2011). Paradoxical function of orexin/hypocretin circuits in a mouse model of Huntington's disease. Neurobiol. Dis. 42, 438-455. doi: 10.1016/j.nbd.2011.02.006
67. Willie, J. T., Chemelli, R. M., Sinton, C. M., Tokita, S., Williams, S. C., Kisanuki, Y. Y., et al. (2003). Distinct narcolepsy syndromes in orexin receptor-2 and orexin null mice: molecular genetic dissection of Non-REM and REM sleep regulatory processes. Neuron 38, 715-730. doi: 10.1016/s0896-6273(03)00330-1
68. Winsky-Sommerer, R., Yamanaka, A., Diano, S., Borok, E., Roberts, A. J., Sakurai, T., et al. (2004). Interaction between the corticotropin-releasing factor system and hypocretins (orexins): a novel circuit mediating stress response. J. Neurosci. 24, 11439-11448. doi: 10.1523/jneurosci.3459-04.2004
69. Yamanaka, A., Beuckmann, C. T., Willie, J. T., Hara, J., Tsujino, N., Mieda, M., et al. (2003a). Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38, 701-713. doi: 10.1016/s0896-6273(03)00331-3
70. Yamanaka, A., Muraki, Y., Tsujino, N., Goto, K., and Sakurai, T. (2003b). Regulation of orexin neurons by the monoaminergic and cholinergic systems. Biochem. Biophys. Res. Commun. 303, 120-129. doi: 10.1016/s0006-291x(03)00299-7
71. Yamanaka, A., Tabuchi, S., Tsunematsu, T., Fukazawa, Y., and Tominaga, M. (2010). Orexin directly excites orexin neurons through orexin 2 receptor. J. Neurosci. 30, 12642-12652. doi: 10.1523/JNEUROSCI.2120-10.2010
72. Yamanaka, A., Tsujino, N., Funahashi, H., Honda, K., Guan, J. L., Wang, Q. P., et al. (2002). Orexins activate histaminergic neurons via the orexin 2 receptor. Biochem. Biophys. Res. Commun. 290, 1237-1245. doi: 10.1006/bbrc.2001.6318
73. Yeo, G. S., and Heisler, L. K. (2012). Unraveling the brain regulation of appetite: lessons from genetics. Nat. Neurosci. 15, 1343-1349. doi: 10.1038/nn.3211
74. Yi, T. M., Huang, Y., Simon, M. I., and Doyle, J. (2000). Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc. Natl. Acad. Sci. U S A 97, 4649-4653. doi: 10.1073/pnas.97.9.4649