Changes in emotional behavior produced by orexin microinjections in the paraventricular nucleus of the thalamus

Pharmacology Biochemistry and Behavior

Volumn 95, Issue 1, 2010, Pages 121-128

  Li, Yonghui ^a,c   Li, Sa ^c   Wei, Chuguang ^a,b   Wang, Huiying ^a,b   Sui, Nan ^a   Kirouac, Gilbert J ^c  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Arousal; Emotion; Hypocretin; Midline thalamus; Motivation; Orexin; Paraventricular nucleus of the thalamus; Thalamus

Indexed keywords

OREXIN A; OREXIN B;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; AVERSION; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DRUG MECHANISM; EMOTION; EMOTIONALITY; ETHOLOGY; FREEZING; GROOMING; LOCOMOTION; MALE; MICROINJECTION; MOTIVATION; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; REARING; THALAMUS MIDLINE NUCLEUS;

ANIMALS; BEHAVIOR, ANIMAL; EMOTIONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICROINJECTIONS; MIDLINE THALAMIC NUCLEI; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 77249169672     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2009.12.016     Document Type: Article

References (65)

1. Alheid G.F. Extended amygdala and basal forebrain. Ann N Y Acad Sci 2003, 985:185-205.
2. Alheid G.F., Heimer L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 1988, 27:1-39.
3. Amygdala and extended amygdala 1995, Academic, San Diego. G.F. Alheid, J.S. de Olmos, C.A. Beltramino (Eds.).
4. Bayer L., Eggermann E., Saint-Mleux B., Machard D., Jones B.E., Muhlethaler M., et al. Selective action of orexin (hypocretin) on nonspecific thalamocortical projection neurons. J Neurosci 2002, 22:7835-7839.
5. Beck C.H., Fibiger H.C. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 1995, 15:709-720.
6. Berendse H.W., Groenewegen H.J. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 1991, 42:73-102.
7. Berendse H.W., Galis-de Graaf Y., Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 1992, 316:314-347.
8. Berridge C.W., Mitton E., Clark W., Roth R.H. Engagement in a non-escape (displacement) behavior elicits a selective and lateralized suppression of frontal cortical dopaminergic utilization in stress. Synapse 1999, 32:187-197.
9. Bhatnagar S., Dallman M.F. The paraventricular nucleus of the thalamus alters rhythms in core temperature and energy balance in a state-dependent manner. Brain Res 1999, 851:66-75.
10. Bhatnagar S., Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 1998, 84:1025-1039.
11. Bhatnagar S., Viau V., Chu A., Soriano L., Meijer O.C., Dallman M.F. A cholecystokinin-mediated pathway to the paraventricular thalamus is recruited in chronically stressed rats and regulates hypothalamic-pituitary-adrenal function. J Neurosci 2000, 20:5564-5573.
12. Bhatnagar S., Huber R., Nowak N., Trotter P. Lesions of the posterior paraventricular thalamus block habituation of hypothalamic-pituitary-adrenal responses to repeated restraint. J Neuroendocrinol 2002, 14:403-410.
13. Bhatnagar S., Huber R., Lazar E., Pych L., Vining C. Chronic stress alters behavior in the conditioned defensive burying test: role of the posterior paraventricular thalamus. Pharmacol Biochem Behav 2003, 76:343-349.
14. Bubser M., Deutch A.Y. Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites. Synapse 1999, 32:13-22.
15. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002, 26:321-352.
16. Carey R.J., Damianopoulos E.N., Shanahan A.B. Cocaine effects on behavioral responding to a novel object placed in a familiar environment. Pharmacol Biochem Behav 2008, 88:265-271.
17. Carter M.E., Borg J.S., de Lecea L. The brain hypocretins and their receptors: mediators of allostatic arousal. Curr Opin Pharmacol 2009, 9:39-45.
18. Chastrette N., Pfaff D.W., Gibbs R.B. Effects of daytime and nighttime stress on Fos-like immunoreactivity in the paraventricular nucleus of the hypothalamus, the habenula, and the posterior paraventricular nucleus of the thalamus. Brain Res 1991, 563:339-344.
19. Cullinan W.E., Helmreich D.L., Watson S.J. Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neurol 1996, 368:88-99.
20. Dai H., Carey R.J. A new method to quantify behavioral attention to a stimulus object in a modified open-field. J Neurosci Methods 1994, 53:29-34.
21. Date Y., Ueta Y., Yamashita H., Yamaguchi H., Matsukura S., Kangawa K., et al. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci U S A 1999, 96:748-753.
22. Davis M., Shi C. The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann N Y Acad Sci 1999, 877:281-291.
23. de Kloet E.R. Hormones, brain and stress. Endocr Regul 2003, 37:51-68.
24. de Olmos J.S., Beltramino C.A., Alheid G.F. Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. The rat nervous system 2004, 509-603. Academic Press, New York. G. Paxinos (Ed.).
25. Dunn A.J., Green E.J., Isaacson R.L. Intracerebral adrenocorticotropic hormone mediates novelty-induced grooming in the rat. Science 1979, 203:281-283.
26. Dunn A.J., Berridge C.W., Lai Y.I., Yachabach T.L. CRF-induced excessive grooming behavior in rats and mice. Peptides 1987, 8:841-844.
27. Endres T., Apfelbach R., Fendt M. Behavioral changes induced in rats by exposure to trimethylthiazoline, a component of fox odor. Behav Neurosci 2005, 119:1004-1010.
28. Espejo E.F. Effects of weekly or daily exposure to the elevated plus-maze in male mice. Behav Brain Res 1997, 87:233-238.
29. Frewen P.A., Lanius R.A. Toward a psychobiology of posttraumatic self-dysregulation: reexperiencing, hyperarousal, dissociation, and emotional numbing. Ann N Y Acad Sci 2006, 1071:110-124.
30. Groenewegen H.J., Berendse H.W. The specificity of the 'nonspecific' midline and intralaminar thalamic nuclei. Trends Neurosci 1994, 17:52-57.
31. Hamlin A.S., Clemens K.J., Choi E.A., McNally G.P. Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur J Neurosci 2009, 29:802-812.
32. Heimer L.A. new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 2003, 160:1726-1739.
33. Hsu D.T., Price J.L. Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 2009, 512:825-848.
34. Huang H., Ghosh P., van den Pol A.N. Prefrontal cortex-projecting glutamatergic thalamic paraventricular nucleus-excited by hypocretin: a feedforward circuit that may enhance cognitive arousal. J Neurophysiol 2006, 95:1656-1668.
35. Ishibashi M., Takano S., Yanagida H., Takatsuna M., Nakajima K., Oomura Y., et al. Effects of orexins/hypocretins on neuronal activity in the paraventricular nucleus of the thalamus in rats in vitro. Peptides 2005, 26:471-481.
36. Jaferi A., Bhatnagar S. Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 2006, 147:4917-4930.
37. Jaferi A., Nowak N., Bhatnagar S. Negative feedback functions in chronically stressed rats: role of the posterior paraventricular thalamus. Physiol Behav 2003, 78:365-373.
38. Kirouac GJ, Li S. Anatomical and functional relationship between the paraventricular nucleus of the thalamus and dynorphin neurons in the nucleus accumbens. Program No. 63.19, Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2008. Online.
39. Kirouac G.J., Parsons M.P., Li S. Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus. Brain Res 2005, 1059:179-188.
40. Klemenhagen K.C., Gordon J.A., David D.J., Hen R., Gross C.T. Increased fear response to contextual cues in mice lacking the 5-HT1A receptor. Neuropsychopharmacology 2006, 31:101-111.
41. Kolaj M., Doroshenko P., Yan Cao X., Coderre E., Renaud L.P. Orexin-induced modulation of state-dependent intrinsic properties in thalamic paraventricular nucleus neurons attenuates action potential patterning and frequency. Neuroscience 2007, 147:1066-1075.
42. Koob G.F. Neuroadaptive mechanisms of addiction: studies on the extended amygdala. Eur Neuropsychopharmacol 2003, 13:442-452.
43. Li S., Kirouac G.J. Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 2008, 506:263-287.
44. Li Y., Li S., Sui N., Kirouac G.J. Orexin-A acts on the paraventricular nucleus of the midline thalamus to inhibit locomotor activity in rats. Pharmacol Biochem Behav 2009, 93:506-514.
45. Marcus J.N., Aschkenasi C.J., Lee C.E., Chemelli R.M., Saper C.B., Yanagisawa M., et al. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 2001, 435:6-25.
46. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol 1955, 48:254-260.
47. Novak C.M., Nunez A.A. Daily rhythms in Fos activity in the rat ventrolateral preoptic area and midline thalamic nuclei. Am J Physiol 1998, 275:R1620-R1626.
48. Novak C.M., Harris J.A., Smale L., Nunez A.A. Suprachiasmatic nucleus projections to the paraventricular thalamic nucleus in nocturnal rats (Rattus norvegicus) and diurnal nile grass rats (Arviacanthis niloticus). Brain Res 2000, 874:147-157.
49. Novak C.M., Smale L., Nunez A.A. Rhythms in Fos expression in brain areas related to the sleep-wake cycle in the diurnal Arvicanthis niloticus. Am J Physiol Regul Integr Comp Physiol 2000, 278:R1267-R1274.
50. Parsons M.P., Li S., Kirouac G.J. The paraventricular nucleus of the thalamus as an interface between the orexin and CART peptides and the shell of the nucleus accumbens. Synapse 2006, 59:480-490.
51. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, San Diego. Fifth Edition.
52. Peng Z.C., Grassi-Zucconi G., Bentivoglio M. Fos-related protein expression in the midline paraventricular nucleus of the rat thalamus: basal oscillation and relationship with limbic efferents. Exp Brain Res 1995, 104:21-29.
53. Pfaff D. Brain Arousal and Information Theory 2006, Harvard University Press, Cambridge, Massachusetts.
54. Pivina S.G., Akulova V.K., Ordyan N.E. Characteristics of behavior and stress reactivity of the hypophyseal-adrenocortical system in rats with prenatal inhibition of testosterone metabolism. Neurosci Behav Physiol 2007, 37:53-58.
55. Ramos A., Mormede P. Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav Rev 1998, 22:33-57.
56. Roseboom P.H., Nanda S.A., Bakshi V.P., Trentani A., Newman S.M., Kalin N.H. Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 2007, 32:44-55.
57. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 2007, 8:171-181.
58. Spruijt B.M., van Hooff J.A., Gispen W.H. Ethology and neurobiology of grooming behavior. Physiol Rev 1992, 72:825-852.
59. Suzuki M., Beuckmann C.T., Shikata K., Ogura H., Sawai T. Orexin-A (hypocretin-1) is possibly involved in generation of anxiety-like behavior. Brain Res 2005, 1044:116-121.
60. Thorpe A.J., Mullett M.A., Wang C., Kotz C.M. Peptides that regulate food intake: regional, metabolic, and circadian specificity of lateral hypothalamic orexin A feeding stimulation. Am J Physiol Regul Integr Comp Physiol 2003, 284:R1409-R1417.
61. Timofeeva E., Richard D. Activation of the central nervous system in obese Zucker rats during food deprivation. J Comp Neurol 2001, 441:71-89.
62. 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 2002, 39:107-140.
63. Vertes R.P., Hoover W.B. Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 2008, 508:212-237.
64. Yehuda R., LeDoux J. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 2007, 56:19-32.
65. Young C.D., Deutch A.Y. The effects of thalamic paraventricular nucleus lesions on cocaine-induced locomotor activity and sensitization. Pharmacol Biochem Behav 1998, 60:753-758.