Hypocretin-1 dose-dependently modulates maternal behaviour in mice

Journal of Neuroendocrinology

Volumn 18, Issue 8, 2006, Pages 553-566

  D'Anna, Kimberly L ^a,b   Gammie, S C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Zoology Research   (United States)

Author keywords

Bed nucleus of the stria terminalis; Grooming; Lateral septum; Maternal care; Maternal defence

Indexed keywords

OREXIN A; PROTEIN C FOS;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GROOMING; LACTATION; LICKING; MALE; MATERNAL ATTITUDE; MATERNAL CARE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; STATISTICAL SIGNIFICANCE;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BENZOXAZOLES; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; INJECTIONS, INTRAVENTRICULAR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LACTATION; MATERNAL BEHAVIOR; MICE; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; UREA;

EID: 33745728415     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2006.01448.x     Document Type: Article

References (65)

1. Levin R, Stern JM. Maternal influences on ontogeny of suckling and feeding rhythms in the rat. J Comp Physiol Psychol 1975; 89: 711-721.
2. Leon M, Woodside B. Energetic limits on reproduction: Maternal food intake. Physiol Behav 1983; 30: 945-957.
3. Stern JM, Levin R. Food availability as a determinant of the rats' circadian rhythm in maternal behavior. Dev Psych 1976; 9: 137-148.
4. Chiang C, Johnson R, Nielsen M. Maternal behavior in mice selected for large litter size. Appl Anim Behav Sci 2002; 79: 63-73.
5. Nishihara K, Horiuchi S. Changes in sleep patterns of young women from late pregnancy to postpartum: Relationships to their infants' movements. Percept Mot Skills 1998; 87: 1043-1056.
6. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, Benham CD, Taylor SG, Routledge C, Hemmati P, Munton RP, Ashmeade TE, Shah AS, Hatcher JP, Hatcher PD, Jones DN, Smith MI, Piper DC, Hunter AJ, Porter RA, Upton N. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci USA 1999; 96: 10911-10916.
7. España RA, Baldo BA, Kelley AE, Berridge CW. Wake-promoting and sleep-suppressing actions of hypocretin (orexin): Basal forebrain sites of action. Neuroscience 2001; 106: 669-715.
8. Piper DC, Upton N, Smith MI, Hunter AJ. The novel brain neuropeptide, orexin-A, modulates the sleep-wake cycle of rats. Eur J Neurosci 2000; 12: 726-730.
9. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999; 98: 437-451.
10. España R, Berridge C, Gammie S. Diurnal levels of Fos immunoreactivity are elevated within hypocretin neurons in lactating mice. Peptides 2004; 25: 1927-1934.
11. Wang J, Murata T, Narita K, Kazumasa H, Higuchi T. Variation in the expression of orexin and orexin receptors in the rat hypothalamus during the estrous cycle. Endocrine 2003; 22: 127-134.
12. Samson WK, Taylor MT. Hypocretin/orexin suppresses corticotroph responsiveness in vitro. Am J Physiol Regul Integr Comp Physiol 2001; 281: R1140-R1145.
13. Taheri S, Bloom SR. Orexins/hypocretins: Waking up the scientific world. Clin Endocrinol 2001; 54: 421-429.
14. Numan M, Insel TR. The Neurobiology of Parental Behavior. New York, NY: Springer-Verlag, 2003.
15. España RA, Valentino RJ, Berridge CW. Fos immunoreactivity in hypocretin-synthesizing and hypocretin-1 receptor-expressing neurons: effects of diurnal and nocturnal spontaneous waking, stress and hypocretin-1 administration. Neuroscience 2003; 121: 201-217.
16. Jasberenyi M, Bujdoso E, Pataki I, Telegdy G. Effects of orexin on the hypothalamic-pituitary-adrenal system. J Endocrinol 2000; 12: 1174-1178.
17. Gammie SC, Negron A, Newman SM, Rhodes JS. Corticotropin-releasing factor inhibits maternal aggression in mice. Behav Neurosci 2004; 118: 805-814.
18. Pedersen CA, Caldwell JD, McGuire M, Evans DL. Corticotropin-releasing hormone inhibits maternal behavior and induces pup-killing. Life Sci 1991; 48: 1537-1546.
19. D'Anna K, Stevenson SA, Gammie S. Urocortin 1 and 3 impair maternal defense behavior in mice. Behav Neurosci 2005; 119: 1061-1071.
20. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 1998; 95: 5335-5340.
21. Bourgin P, Huitron-Resendiz S, Spier AD, Fabre V, Morte B, Criado JR, Sutcliffe J, Henriksen SJ, de Lecea L. Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons. J Neurosci 2000; 20: 7760-7765.
22. Ishii Y, Blundell J, Halford J, Upton N, Porter R, Johns A, Jeffrey P, Summerfield S, Rodgers RJ. Anorexia and weight loss in male rates 24h following single dose treatment with orexin-1 receptor antagonist SB-334867. Behav Brain Res 2005; 157: 331-341.
23. Rodgers RJ, Halford J, Nunes de Souza R, Canto de Souza A, Piper DC, Arch J, Upton N, Porter R, Johns A, Blundell J. SB-334867, a selective orexin-1 receptor antagonist, enhances behavioral satiety and blocks the hyperphagic effect of orexin-A in rats. Eur J Neurosci 2001; 13: 1444-1452.
24. Svare B, Betteridge C, Katz D, Samuels O. Some situational and experiential determinants of maternal aggression in mice. Physiol Behav 1981; 26: 253-258.
25. Gammie SC, Huang PL, Nelson RJ. Maternal aggression in endothelial nitric oxide synthase-deficient mice. Hormones Behav 2000; 38: 13-20.
26. Gammie SC, Nelson RJ. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J Neurosci 1999; 19: 8027-8035.
27. Myers MM, Brunelli SA, Squire JM, Shindeldecker RD, Hofer MA. Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 1989; 22: 29-53.
28. Champagne F, Francis D, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003; 79: 359-371.
29. Dabney A, Storey JD. QVALUE. Available at: http://facultywashingtonedu/~jstorey/qvalue/.
30. Rhodes JS, Ryabinin A, Crabbe J. Patterns of brain activation associated with contextual conditioning to methamphetamine in mice. Behav Neurosci 2005; 119: 759-771.
31. Day H, Masini C, Campeau S. The pattern of brain c-fos mRNA induced by a component of fox odor, 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systematic and processive stress characteristics. Brain Res 2004; 1025: 139-151.
32. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997; 277: 1659-1662.
33. Francis D, Diorio J, Liu D, Meaney MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999; 286: 1155-1158.
34. Ida T, Nakahara K, Murakami N, Nakazato M. Effect of lateral cerebroventricular injection of the appetite-stimulating neuropeptide, orexin and neuropeptide Y, on the various behavioral activities of rats. Brain Res 1999; 821: 526-529.
35. Mileykovskiy B, Kiyashchenko L, Siegel J. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005; 46: 787-798.
36. Vittoz N, Berridge CW. Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: Involvement of the ventral tegmental area. Neuropsychopharmacology 2006; 31: 384-395.
37. Peyron C, Tighe D, van de Poll NA, De Lecea L, Heller H, Sutcliffe J, Kilduff T. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 1998; 18: 9996-10015.
38. Champagne F, Chretien P, Stevenson C, Zhang T, Gratton A, Meaney MJ. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci 2004; 24: 4113-4123.
39. Matsuzaki I, Sakurai T, Kunii K, Nakamura T, Yanagisawa M, Goto K. Involvement of serotonergic system in orexin-induced behavioral alterations in rats. Regul Pept 2002; 104: 119-123.
40. Duxon M, Stretton J, Starr K, Jones DN, Holland V, Riley G, Jerman J, Brough S, Smart D, Johns A, Chan W, Porter R, Upton N. Evidence that orexin-A-evoked grooming in the rat is mediated by orexin-1 (OX1) receptors, with downstream 5-HT2C receptor involvement. Psychopharmacology (Berl) 2001; 153: 203-209.
41. Pedersen CA, Vadlamudi SV, Boccia ML, Amico JA. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes, Brain and Behavior 2006; 5: 274-281.
42. Pedersen CA, Boccia ML. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol Behav 2003; 80: 233-241.
43. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski G, Wilson S, Arch J, Buckingham R, Haynes A, Carr S, Annan R, McNulty D, Liu W-S, Terrett J, Elshourbagy N, Bergsma D, Yanagisawa M. Orexin and orexin receptors. A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998; 92: 573-585.
44. Siegel J. Hypocretin (orexin). Role in normal behavior and neuropathology. Annu Rev Psychol 2004; 55: 125-148.
45. Sakurai T. Roles of orexin/hypocretin in regulation of sleep/wakefulness and energy homeostasis. Sleep Med Rev 2005; 9: 231-241.
46. Samson WK, Resch Z. The hypocretin/orexin story. Trends Endocrinol Metabolism 2000; 11: 257-262.
47. Trivedi PYuH, MacNeil D, Van der Ploeg L, Guan X. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 1998; 438: 71-75.
48. Marcus J, Aschkenasi C, Lee C, Chemelli RM, Saper CB, Yanagisawa M, Elmquist JK. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 2001; 435: 6-25.
49. Stricker-Krongrad A, Beck B. Modulation of hypothalamic hypocretin/ orexin mRNA expression by glucocorticoids. Biochem Biophys Res Commun 2002; 296: 129-133.
50. Paneda C, Winsky-Sommerer R, Boutrel B, De Lecea L. The corticotropin-releasing factor-hypocretin connection: Implications in stress response and addiction. Drug News Perspect 2005; 18: 250-255.
51. Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Hormones Behav 2004; 46: 411-419.
52. Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on induction of maternal behavior in the virgin female rat. Hormones Behav 2006; 49: 337-345.
53. Consiglio AR, Borsoi A, Pereira GA, Lucion AB. Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol Behav 2005; 85: 354-362.
54. Lubin DA, Elliott JC, Black MC, Johns JM. An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 2003; 117: 195-201.
55. Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID. Brain oxytocin correlates with maternal aggression: Link to anxiety. J Neurosci 2005; 25: 6807-6815.
56. Ishii Y, Blundell J, Halford J, Upton N, Porter R, Johns A, Rodgers RJ. Differential effects of the selective orexin-1 receptor antagonist SB-334867 and lithium chloride on the behavioural satiety sequence in rats. Physiol Behav 2004; 81: 129-140.
57. Sheehan T, Cirrito J, Numan M, Numan M. Using c-Fos immunocytochemistry to identify forebrain regions that may inhibit maternal behavior in rats. Behav Neurosci 2000; 114: 337-352.
58. Calamandrei G, Keverne EB. Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience. Behav Neurosci 1994; 108: 113-120.
59. Lee A, Clancy S, Fleming AS. Mother rats bar-press for pups: Effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup reinforcement. Behav Brain Res 2000; 108: 215-231.
60. Harris GC, Wimmer M, Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005; 437: 556-559.
61. Thompson A, Kristal MB. Opiod stimulation in the ventral tegmental area facilitates the onset of maternal behavior in rats. Brain Res 1996; 743: 184-201.
62. Mattson B, Williams S, Rosenblatt JS, Morrell JI. Comparison of two positive reinforcing stimuli: Pups and cocaine throughout the postpartum period. Behav Neurosci 2001; 115: 683-694.
63. Insel TR. Is social attachment an addictive disorder? Physiol Behav 2003; 79: 184-186.
64. De Lecea L, Kilduff T, Peyron C, Gao X-B, Foye P, Danielson P, Fukuhara C, Battenberg E, Gautvik V, Bartlett IIF, Frankel W, van den Pol A, Bloom FE, Gautvik K, Sutcliffe J. The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 1998; 95: 322-327.
65. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Amsterdam: Elsevier, 2001.