Orexin/Hypocretin-1 Receptor Antagonism Selectively Reduces Cue-Induced Feeding in Sated Rats and Recruits Medial Prefrontal Cortex and Thalamus

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Cole, Sindy ^a   Mayer, Heather S ^a   Petrovich, Gorica D ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1-(2-METHYLBENZOXAZOL-6-YL)-3-(1,5)NAPHTHYRIDIN-4-YL UREA; BENZOXAZOLE DERIVATIVE; OREXIN; OREXIN RECEPTOR; OREXIN RECEPTOR ANTAGONIST; UREA;

AMYGDALA; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; ASSOCIATION; DRUG EFFECTS; EATING; FEEDING BEHAVIOR; LEARNING; METABOLISM; PREFRONTAL CORTEX; RAT; REWARD; THALAMUS;

AMYGDALA; ANIMALS; BENZOXAZOLES; CUES; EATING; FEEDING BEHAVIOR; LEARNING; OREXIN RECEPTOR ANTAGONISTS; OREXIN RECEPTORS; OREXINS; PREFRONTAL CORTEX; RATS; REWARD; THALAMUS; UREA;

EID: 84946594671     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16143     Document Type: Article

References (54)

1. Birch, L. L, McPhee, L., Sullivan, S. & Johnson, S. Conditioned meal initiation in young children. Appetite 13, 105-113 (1989).
2. Cornell, C. E., Rodin, J. & Weingarten, H. Stimulus-induced eating when satiated. Physiol. Behav. 45, 695-704 (1989).
3. Petrovich, G. D. Forebrain networks and the control of feeding by environmental learned cues. Physiol. Behav. 121, 10-18 (2013).
4. Petrovich, G. D., Setlow, B., Holland, P. C. & Gallagher, M. Amygdalo-hypothalamic circuit allows learned cues to override satiety and promote eating. J. Neurosci. 22, 8748-8753 (2002).
5. Petrovich, G. D., Ross, C. A., Holland, P. C. & Gallagher, M. Medial prefrontal cortex is necessary for an appetitive contextual conditioned stimulus to promote eating in sated rats. J. Neurosci. 27, 6436-6441 (2007).
6. Petrovich, G. D., Holland, P. C. & Gallagher, M. Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J. Neurosci. 25, 8295-8302 (2005).
7. de Lecea, L. et al. The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. USA 95, 322-327 (1998).
8. Sakurai, T. et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585 (1998).
9. Peyron, C. et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996-10015 (1998).
10. Rodgers, R. J. et al. Dose-response effects of orexin-A on food intake and the behavioural satiety sequence in rats. Regul. Pept. 96, 71-84 (2000).
11. Choi, D. L., Davis, J. F., Fitzgerald, M. E. & Benoit, S. C. The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience 167, 11-20 (2010).
12. Harris, G. C., Wimmer, M. & Aston-Jones, G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437, 556-559 (2005).
13. Petrovich, G. D., Hobin, M. P. & Reppucci, C. J. Selective Fos induction in hypothalamic orexin/hypocretin, but not melaninconcentrating hormone neurons, by a learned food-cue that stimulates feeding in sated rats. Neuroscience 224, 70-80 (2012).
14. Nair, S. G., Golden, S. A. & Shaham, Y. Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br. J. Pharmacol. 154, 406-416 (2008).
15. Cason, A. M. & Aston-Jones, G. Role of orexin/hypocretin in conditioned sucrose-seeking in rats. Psychopharmacology (Berl) 226, 155-165 (2013a).
16. Cason, A. M. & Aston-Jones, G. Attenuation of saccharin-seeking in rats by orexin/hypocretin receptor 1 antagonist. Psychopharmacology (Berl) 228, 499-507 (2013b).
17. Borgland, S. L. et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J. Neurosci. 29, 11215-11225 (2009).
18. Marcus, J. N. et al. Differential expression of orexin receptors 1 and 2 in the rat brain. J. Comp. Neurol. 435, 6-25 (2001).
19. Trivedi, P., Yu, H., MacNeil, D. J., Van der Ploeg, L. H. & Guan, X. M. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett. 438, 71-75 (1998).
20. Akanmu, M. A. & Honda, K. Selective stimulation of orexin receptor type 2 promotes wakefulness in freely behaving rats. Brain Res. 1048, 138-145 (2005).
21. Cason, A. M. et al. Role of orexin/hypocretin in reward-seeking and addiction: implications for obesity. Physiol. Behav. 100. 419-428 (2010).
22. Willie, J. T. et al. 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 (2002).
23. Haynes, A. C. et al. A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul. Pept. 96, 45-51 (2000).
24. Choi, D. L. et al. Orexin signaling in the paraventricular thalamic nucleus modulates mesolimbic dopamine and hedonic feeding in the rat. Neuroscience 210, 243-248 (2012).
25. Sharf, R. et al. Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol. Psychiatry 67, 753-760 (2010).
26. Richards, J. K. et al. Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology (Berl) 199, 3109-117 (2008).
27. Schmitt, O. et al. Orexinergic innervation of the extended amygdala and basal ganglia in the rat. Brain Struct. Funct. 217, 233-256 (2012).
28. Risco, S. & Mediavilla, C. Orexin-1 receptor antagonist in central nucleus of the amygdala attenuates the acquisition of flavortaste preference in rats. Pharmacol. Biochem. Behav. 126, 7-12 (2014).
29. Rodgers, R. J. et al. SB-334867, a selective orexin-1 receptor antagonist, enhances behavioural satiety and blocks the hyperphagic effect of orexin-A in rats. Eur. J. Neurosci. 13, 1444-1452 (2001).
30. Saper, C. B. Staying awake for dinner: hypothalamic integration of sleep, feeding, and circadian rhythms. Prog. Brain Res. 153, 243-252 (2006).
31. Mahler, S.V., Moorman, D.E., Smith, R.J., James, M.H. & Aston-Jones, G. J. Motivational activation: a unifying hypothesis of orexin/hypocretin function. Nat Neurosci. 17, 1298-303. (2014).
32. Sakurai, T. The role of orexin in motivated behaviours. Nat Rev Neurosci. 15, 719-31. (2014).
33. Burgos-Robles, A., Bravo-Rivera, H. & Quirk, G. J. Prelimbic and infralimbic neurons signal distinct aspects of appetitive instrumental behavior. PLoS ONE 8, e57575. doi: 10.1371/journal.pone.0057575 (2013).
34. Calu, D. J. et al. Optogenetic inhibition of dorsal medial prefrontal cortex attenuates stress-induced reinstatement of palatable food seeking in female rats. J. Neurosci. 33, 214-226 (2013).
35. Nair, S. G. et al. Role of dorsal medial prefrontal cortex dopamine D1-family receptors in relapse to high-fat food seeking induced by the anxiogenic drug yohimbine. Neuropsychopharmacology 36, 497-510 (2011).
36. Van der Werf, Y. D., Witter, M. P. & Groenewegen, H. J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39, 107-140 (2002).
37. Vertes, R. P., Linley, S. B. & Hoover, W. B. Limbic circuitry of the midline thalamus. Neurosci. Biobehav. Rev. e-pub ahead of print 20 January 2015. doi: 10.1016/j.neubiorev.2015.01.014 (2015).
38. Colavito, V., Tesoriero, C., Wirtu, A. T., Grassi-Zucconi, G. & Bentivoglio, M. Limbic thalamus and state-dependent behavior: The paraventricular nucleus of the thalamic midline as a node in circadian timing and sleep/wake-regulatory networks. Neurosci. Biobehav. Rev. e-pub ahead of print 3 December 2014. doi: 10.1016/j.neubiorev.2014.11.021 (2014).
39. Hsu, D. T., Kirouac, G. J., Zubieta, J. K. & Bhatnagar, S. Contributions of the paraventricular thalamic nucleus in the regulation of stress, motivation, and mood. Front. Behav. Neurosci. 8, 73. doi: 10.3389/fnbeh.2014.00073 (2014).
40. Aracri, P., Banfi, D., Pasini, M. E., Amadeo, A. & Becchetti, A. Hypocretin (orexin) regulates glutamate input to fast-spiking interneurons in layer V of the Fr2 region of the murine prefrontal cortex. Cereb. Cortex; e-pub ahead of print 1 December 2013. doi: 10.1093/cercor/bht326. (2013).
41. Burdakov, D., Liss, B. & Ashcroft, F.M. Orexin excites GABAergic neurons of the arcuate nucleus by activating the sodium-calcium exchanger. J. Neurosci. 23, 4951-4957 (2003).
42. Wu, M. et al. Hypocretin increases impulse flow in the septohippocampal GABAergic pathway: implications for arousal via a mechanism of hippocampal disinhibition. J. Neurosci. 22, 7754-7765 (2002).
43. Arcelli, P., Frassoni, C., Regondi, M. C., De Biasi, S. & Spreafico, R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res. Bull. 42, 27-37 (1997).
44. Berendse, H. W. & Groenewegen, H. J. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42, 73-102 (1991).
45. Li, S. & Kirouac, G. J. Sources of inputs to the anterior and posterior aspects of the paraventricular nucleus of the thalamus. Brain Struct. Funct. 217, 257-273 (2012).
46. Mayannavar, S., Rashmi, K. S., Rao, Y. D., Yadav, S. & Ganaraja, B. Effect of Orexin-A infusion in to the Nucleus Accumbens on consummatory behaviour and alcohol preference in male Wistar rats. Indian J Physiol Pharmacol. 58, 319-326 (2014).
47. Thorpe, A. J. & Kotz, C.M. Orexin A in the nucleus accumbens stimulates feeding and locomotor activity. Brain Res. 1050, 156-162 (2005).
48. Sweet, D. C., Levine, A. S. & Kotz, C. M. Functional opioid pathways are necessary for hypocretin-1 (orexin-A)-induced feeding. Peptides. 25, 307-314 (2004).
49. Ho, C. Y. & Berridge, K. C. An orexin hotspot in ventral pallidum amplifies hedonic 'liking' for sweetness. Neuropsychopharmacology. 38, 1655-1664 (2013).
50. Cole, S., Powell, D. J. & Petrovich, G. D. Differential recruitment of distinct amygdalar nuclei across appetitive associative learning. Learn. Mem. 20, 295-299 (2013).
51. Swanson, L. W. Brain Maps: Structure of the Rat Brain (Elsevier, 2004).
52. Hahn, J. D. & Swanson, L. W. Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain. Res. Rev. 64, 14-103 (2010).
53. Hahn, J. D. & Swanson, L. W. Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat. J. Comp. Neurol. 520, 1831-1890 (2012).
54. Bird, K. D. Analysis of variance via confidence intervals (Sage, 2004).