Neuropeptide S and BDNF gene expression in the amygdala are influenced by social decision-making under stress

Frontiers in Behavioral Neuroscience

Volumn 8, Issue APR, 2014, Pages

  Smith, Justin P ^a,b,c   Achua, Justin K ^a,b,c   Summers, Tangi R ^a,b   Ronan, Patrick J ^b,c,d   Summers, Cliff H ^a,b  

^a W O Farber Center for Civic Leadership   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c Research Service   (United States)

^d Avera Research Institute   (United States)

Author keywords

Aggression; BDNF; Decision making; Escape; Neuropeptide S; Stress; Submission

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; MESSENGER RNA; NEUROPEPTIDE S;

ADULT; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BASOLATERAL AMYGDALA; BDNF GENE; CENTRAL NUCLEUS (AMYGDALA); CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DECISION MAKING; ESCAPE BEHAVIOR; GENE EXPRESSION; HORMONE DETERMINATION; LATENT PERIOD; MALE; MOUSE; NONHUMAN; NPS GENE; OPEN FIELD BEHAVIOR; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOCIAL BEHAVIOR; SOCIAL DECISION MAKING; SOCIAL INTERACTION; STRESS;

EID: 84898762199     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00121     Document Type: Article

References (83)

1. Alvarez, J., Giuditta, A., and Koenig, E. (2000). Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol. 62, 1-62. doi: 10. 1016/s0301-0082(99)00062-3.
2. Arendt, D. H., Ronan, P. J., Oliver, K. D., Callahan, L. B., Summers, T. R., and Summers, C. H. (2013). Depressive behavior and activation of the orexin/hypocretinsystem. Behav. Neurosci. 127, 86-94. doi: 10.1037/a0031442.
3. Arendt, D. H., Smith, J. P., Bastida, C. C., Prasad, M. S., Oliver, K. D., Eyster, K. M., et al. (2012). Contrasting hippocampal and amygdalar expression of genes related to neural plasticity during escape from social aggression. Physiol. Behav. 107, 670-679. doi: 10.1016/j.physbeh.2012.03.005.
4. Arendt, D. H., Smith, J. P., Summers, T. R., Carpenter, R. E., and Summers, C. H. (2009). Stress coping via aggression, submission and learned escape: 3D behavioral analyses. Soc. Neurosci. Abst. 35, 582-513.
5. Bechara, A., Damasio, H., and Damasio, A. R. (2003). Role of the amygdala in decision-making. Ann. N Y Acad. Sci. 985, 356-369. doi: 10.1111/j.1749-6632. 2003.tb07094.x
6. Bechara, A., Damasio, H., Damasio, A. R., and Lee, G. P. (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decisionmaking. J. Neurosci. 19, 5473-5481.
7. Berton, O., Mcclung, C. A., Dileone, R. J., Krishnan, V., Renthal, W., Russo, S. J., et al. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868. doi: 10.1126/science.1120972.
8. Blanchard, D. C., Summers, C. H., and Blanchard, R. J. (2013). The role ofbehavior in translational models for psychopathology: functionality and dysfunctional behaviors. Neurosci. Biobehav. Rev. 37, 1567-1577. doi: 10.1016/j.neubiorev. 2013.06.008
9. Brand, M., Grabenhorst, F., Starcke, K., Vandekerckhove, M. M., and Markowitsch, H. J. (2007). Role of the amygdala in decisions under ambiguity and decisions under risk: evidence from patients with Urbach-Wiethe disease. Neuropsycholo- gia 45, 1305-1317. doi: 10.1016/j.neuropsychologia.2006.09.021
10. Broad, K. D., Mimmack, M. L., Keverne, E. B., and Kendrick, K. M. (2002). Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory. Eur. J. Neurosci. 16, 2166-2174. doi: 10.1046/j.1460-9568.2002.02311.x
11. Buxbaum, A. R., Wu, B., and Singer, R. H. (2014). Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343, 419-422. doi: 10.1126/science.1242939.
12. Cannella, N., Kallupi, M., Ruggeri, B., Ciccocioppo, R., and Ubaldi, M. (2013). The role of the neuropeptide S system in addiction: focus on its interaction with the CRF and hypocretin/orexin neurotransmission. Prog. Neurobiol. 100, 48-59. doi: 10.1016/j.pneurobio.2012.09.005.
13. Carpenter, R. E., Korzan, W. J., Bockholt, C., Watt, M. J., Forster, G. L., Renner, K. J., et al. (2009a). Corticotropin releasing factor influences aggression and monoamines: modulation of attacks and retreats. Neuroscience 158, 412-425. doi: 10.1016/j.neuroscience.2008.10.014.
14. Carpenter, R. E., Sabirzhanov, B., and Summers, C. H. (2009b). Molecular substrates of social fear conditioning in the hippocampus of rainbow trout. Soc. Neurosci. Abs. 35, 478-479.
15. Carpenter, R. E., and Summers, C. H. (2009). Learning strategies during fear conditioning. Neurobiol. Learn. Mem. 91, 415-423. doi: 10.1016/j.nlm.2009.01.009
16. Colzato, L. S., Van Der Does, A. J., Kouwenhoven, C., Elzinga, B. M., and Hommel, B. (2011). BDNF Val(66)Met polymorphism is associated with higher anticipatory cortisol stress response, anxiety and alcohol consumption in healthy adults. Psychoneuroendocrinology 36, 1562-1569. doi: 10.1016/j.psyneuen.2011.04.010
17. Dannlowski, U., Kugel, H., Franke, F., Stuhrmann, A., Hohoff, C., Zwanzger, P., et al. (2011). Neuropeptide-S (NPS) receptor genotype modulates basolat- eral amygdala responsiveness to aversive stimuli. Neuropsychopharmacology 36, 1879-1885. doi: 10.1038/npp.2011.73
18. da Rocha, F. F., Malloy-Diniz, L., Lage, N. V., and Correa, H. (2011). The relationship between the Met allele of the BDNF Val66Met polymorphism and impairments in decision-making under ambiguity in patients with obsessive- compulsive disorder. Genes Brain Behav. 10, 523-529. doi: 10.1111/j.1601-183x. 2011.00687.x
19. Davis, M. (1980). Neurochemical modulation of sensory-motor reactivity: acoustic and tactile startle reflexes. Neurosci. Biobehav. Rev. 4, 241-263. doi: 10. 1016/0149-7634(80)90016-0.
20. Davis, M. (2006). Neural systems involved in fear and anxiety measured with fear- potentiated startle. Am. Psychol. 61, 741-756. doi: 10.1037/0003-066x.61.8.741.
21. Deglincerti, A., and Jaffrey, S. R. (2012). Insights into the roles of local translation from the axonal transcriptome. Open Biol. 2:120079. doi: 10.1098/rsob.120079
22. de Visser, L., Baars, A. M., Lavrijsen, M., Van Der Weerd, C. M., and Van Den Bos, R. (2011a). Decision-makingperformance is related to levels of anxietyand differential recruitment of frontostriatal areas in male rats. Neuroscience 184, 97-106. doi: 10.1016/j.neuroscience.2011.02.025
23. de Visser, L., Baars, A. M., Van 'T Klooster, J., and Van Den Bos, R. (2011b). Transient inactivation of the medial prefrontal cortex affects both anxiety and decision-making in male wistar rats. Front. Neurosci. 5:102. doi: 10.3389/fnins. 2011.00102
24. de Visser, L., Van Der Knaap, L. J., Van De Loo, A. J., Van Der Weerd, C. M., Ohl, F., and Van Den Bos, R. (2010). Trait anxiety affects decision-making differently in healthy men and women: towards gender-specific endophenotypes of anxiety. Neuropsychologia 48, 1598-1606. doi: 10.1016/j.neuropsychologia.2010.01.027.
25. Diogenes, M. J., Costenla, A. R., Lopes, L. V., Jeronimo-Santos, A., Sousa, V. C., Fontinha, B. M., et al. (2011). Enhancement of LTP in aged rats is dependent on endogenous BDNF. Neuropsychopharmacology 36, 1823-1836. doi: 10. 1038/npp.2011.64
26. Duangdao, D. M., Clark, S. D., Okamura, N., and Reinscheid, R. K. (2009). Behavioral phenotyping ofneuropeptide S receptor knockout mice. Behav. Brain Res. 205, 1-9. doi: 10.1016/j.bbr.2009.07.024.
27. Ebner, K., Rjabokon, A., Pape, H. C., and Singewald, N. (2011). Increased in vivo release of neuropeptide S in the amygdala of freely moving rats after local depolarisation and emotional stress. Amino Acids 41, 991-996. doi: 10. 1007/s00726-011-1058-0.
28. Enquist, J., Ferwerda, M., Madhavan, A., Hok, D., and Whistler, J. L. (2012). Chronic ethanol potentiates the effect of neuropeptide s in the basolateral amygdala and shows increased anxiolytic and anti-depressive effects. Neuropsychopharmacology 37, 2436-2445. doi: 10.1038/npp.2012.102
29. Fanous, S., Hammer, R. P. Jr., and Nikulina, E. M. (2010). Short- and longterm effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions. Neuroscience 167, 598-607. doi: 10.1016/j.neuroscience.2010.02.064.
30. Feder, A., Nestler, E. J., and Charney, D. S. (2009). Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 10, 446-457. doi: 10.1038/nrn2649.
31. Fendt, M., Imobersteg, S., Burki, H., Mcallister, K. H., and Sailer, A. W. (2010). Intra-amygdala injections of neuropeptide S block fear-potentiated startle. Neurosci. Lett. 474, 154-157. doi: 10.1016/j.neulet.2010.03.028.
32. File, S.E., and Hyde, J.R. (1978). Can social interaction be used to measure anxiety? Br. J. Pharmacol. 62, 19-24. doi: 10.1111/j.1476-5381.1978.tb07001.x
33. Gasic, G. P., Smoller, J. W., Perlis, R. H., Sun, M., Lee, S., Kim, B. W., et al. (2009). BDNF, relative preference and reward circuitry responses to emotional communication. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 762-781. doi: 10.1002/ajmg.b.30944.
34. Gourley, S. L., Swanson, A. M., Jacobs, A. M., Howell, J. L., Mo, M., Dileone, R. J., et al. (2012). Action control is mediated byprefrontal BDNF and glucocorticoid receptor binding. Proc. Natl. Acad. Sci. U S A 109, 20714-20719. doi: 10. 1073/pnas.1208342109.
35. Graham, L. K., Yoon, T., and Kim, J. J. (2010). Stress impairs optimal behavior in a waterforagingchoicetaskinrats. Learn Mem. 17, 1-4. doi: 10.1101/lm.1605510.
36. Guerrini, R., Salvadori, S., Rizzi, A., Regoli, D., and Calo, G. (2010). Neurobiology, pharmacologyand medicinal chemistryof neuropeptide S and its receptor. Med. Res. Rev. 30, 751-777. doi: 10.1002/med.20180.
37. Ionescu, I. A., Dine, J., Yen, Y. C., Buell, D. R., Herrmann, L., Holsboer, F., et al. (2012). Intranasally administered neuropeptide S (NPS) exerts anxiolytic effects following internalization into NPS receptor-expressing neurons. Neuropsychopharmacology 37, 1323-1337. doi: 10.1038/npp.2011.317.
38. Jung, H., Yoon, B. C., and Holt, C. E. (2012). Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat. Rev. Neurosci. 13, 308-324. doi: 10.1038/nrn3210.
39. Jungling, K., Liu, X., Lesting, J., Coulon, P., Sosulina, L., Reinscheid, R. K., et al. (2012). Activation of neuropeptide S-expressing neurons in the locus coeruleus by corticotropin-releasing factor. J. Physiol. 590, 3701-3717. doi: 10. 1113/jphysiol.2011.226423.
40. Jungling, K., Seidenbecher, T., Sosulina, L., Lesting, J., Sangha, S., Clark, S.D., et al. (2008). Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala. Neuron 59, 298-310. doi: 10.1016/j.neuron.2008.07.002.
41. Kang, J. I., Namkoong, K., Ha, R. Y., Jhung, K., Kim, Y. T., and Kim, S. J. (2010). Influence ofBDNF and COMT polymorphisms on emotional decision-making. Neuropharmacology 58, 1109-1113. doi: 10.1016/j.neuropharm.2010.02.001.
42. Koolhaas, J. M., De Boer, S. F., Coppens, C. M., and Buwalda, B. (2010). Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front. Neuroendocrinol. 31, 307-321. doi: 10.1016/j.yfrne.2010.04.001.
43. Koolhaas, J. M., De Boer, S. F., De Rutter, A. J., Meerlo, P., and Sgoifo, A. (1997). Social stress in rats and mice. Acta Physiol. Scand. Suppl. 640, 69-72.
44. Koolhaas, J. M., Everts, H., De Ruiter, A. J., De Boer, S. F., and Bohus, B. (1998). Coping with stress in rats and mice: differential peptidergic modulation of the amygdala-lateral septum complex. Prog. Brain Res. 119, 437-448. doi: 10. 1016/s0079-6123(08)61586-1.
45. Koot, S., Baars, A., Hesseling, P., Van Den Bos, R., and Joels, M. (2013). Time- dependent effects of corticosterone on reward-based decision-making in a rodent model of the Iowa Gambling Task. Neuropharmacology 70, 306-315. doi: 10.1016/j.neuropharm.2013.02.008.
46. Koot, S., Zoratto, F., Cassano, T., Colangeli, R., Laviola, G., Van Den Bos, R., et al. (2012). Compromised decision-making and increased gambling proneness following dietary serotonin depletion in rats. Neuropharmacology 62, 1640-1650. doi: 10.1016/j.neuropharm.2011.11.002.
47. Krishnan, V., Han, M. H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., et al. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404. doi: 10.1016/j.cell.2007.09.018.
48. LeDoux, J. E., Cicchetti, P., Xagoraris, A., and Romanski, L. M. (1990). The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci. 10, 1062-1069.
49. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCRand the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
50. Lonsdorf, T. B., Weike, A. I., Golkar, A., Schalling, M., Hamm, A. O., and Ohman, A. (2010). Amygdala-dependent fear conditioning in humans is modulated by the BDNFval66met polymorphism. Behav. Neurosci. 124, 9-15. doi: 10. 1037/a0018261
51. Meis, S., Bergado-Acosta, J. R., Yanagawa, Y., Obata, K., Stork, O., and Munsch, T. (2007). Identification of a neuropeptide S responsive circuitry shaping amygdala activity via the endopiriform nucleus. PLoS One 3:e2695. doi: 10.1371/journal. pone.0002695
52. Monfils, M. H., Cowansage, K. K., and Ledoux, J. E. (2007). Brain-derived neurotrophic factor: linking fear learning to memory consolidation. Mol. Pharmacol. 72, 235-237. doi: 10.1124/mol.107.038232.
53. Morgan, C. A. 3rd, Wang, S., Southwick, S. M., Rasmusson, A., Hazlett, G., Hauger, R. L., et al. (2000). Plasma neuropeptide-Y concentrations in humans exposed to military survival training. Biol. Psychiatry 47, 902-909. doi: 10.1016/s0006- 3223(99)00239-5
54. Okamura, N., Garau, C., Duangdao, D. M., Clark, S. D., Jungling, K., Pape, H. C., et al. (2011). Neuropeptide S enhances memory during the consolidation phase and interacts with noradrenergic systems in the brain. Neuropsychopharmacology 36, 744-752. doi: 10.1038/npp.2010.207.
55. Orsini, C. A., and Maren, S. (2012). Neural and cellular mechanisms of fear and extinction memory formation. Neurosci. Biobehav. Rev. 36, 1773-1802. doi: 10. 1016/j.neubiorev.2011.12.014.
56. Palkovits, M. (1973). Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 59,449-450. doi: 10.1016/0006-8993(73)90290-4.
57. Pape, H. C., Jungling, K., Seidenbecher, T., Lesting, J., and Reinscheid, R. K. (2010). Neuropeptide S: a transmitter system in the brain regulating fear and anxiety. Neuropharmacology 58, 29-34. doi: 10.1016/j.neuropharm.2009.06.001.
58. Park, C. R., Campbell, A. M., and Diamond, D. M. (2001). Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats. Biol. Psychiatry 50, 994-1004. doi: 10.1016/s0006-3223(01)01255-0.
59. Park, H. Y., Lim, H., Yoon, Y. J., Follenzi, A., Nwokafor, C., Lopez-Jones, M., et al. (2014). Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 343, 422-424. doi: 10.1126/science.1239200.
60. Paxinos, G., and Franklin, K. B. J. (2004). The Mouse Brain in Stereotaxic Coordinates. Amsterdam, Boston: Elsevier Academic Press.
61. Piper, M., and Holt, C. (2004). RNA translation in axons. Annu. Rev. Cell Dev. Biol. 20, 505-523. doi: 10.1146/annurev.cellbio.20.010403.111746.
62. Pizarro, J. M., Lumley, L. A., Medina, W., Robison, C. L., Chang, W. E., Alagappan, A., et al. (2004). Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res. 1025, 10-20. doi: 10.1016/j. brainres.2004.06.085
63. Ramos, A., Berton, O., Mormede, P., and Chaouloff, F. (1997). A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav. Brain Res. 85, 57-69. doi: 10.1016/s0166-4328(96)00164-7.
64. Rattiner, L. M., Davis, M., French, C. T., and Ressler, K. J. (2004). Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala- dependent fear conditioning. J. Neurosci. 24, 4796-4806. doi: 10.1523/jneurosci. 5654-03.2004
65. Razzoli, M., Domenici, E., Carboni, L., Rantamaki, T., Lindholm, J., Castren, E., et al. (2011). A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress. Genes Brain Behav. 10, 424-433. doi: 10. 1111/j.1601-183x.2011.00681.x
66. Roth, T. L., Zoladz, P. R., Sweatt, J. D., and Diamond, D. M. (2011). Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. J. Psychiatr. Res. 45, 919-926. doi: 10.1016/j. jpsychires.2011.01.013.
67. Ruzza, C., Pulga, A., Rizzi, A., Marzola, G., Guerrini, R., and Calo, G. (2012). Behavioural phenotypic characterization of CD-1 mice lacking the neuropeptide S receptor. Neuropharmacology 62, 1999-2009. doi: 10.1016/j.neuropharm.2011.12.036
68. Schenkel, L. C., Segal, J., Becker, J. A., Manfro, G. G., Bianchin, M. M., and Leistner-Segal, S. (2010). The BDNF Val66Met polymorphism is an independent risk factor for high lethality in suicide attempts of depressed patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 940-944. doi: 10.1016/j.pnpbp.2010. 04.023
69. Shafiei, N., Gray, M., Viau, V., and Floresco, S. B. (2012). Acute stress induces selective alterations in cost/benefit decision-making. Neuropsychopharmacology 37, 2194-2209. doi: 10.1038/npp.2012.69
70. Smagin, G. N., Harris, R. B., and Ryan, D. H. (1996). Corticotropin-releasing factor receptor antagonist infused into the locus coeruleus attenuates immobilization stress-induced defensive withdrawal in rats. Neurosci. Lett. 220, 167-170. doi: 10. 1016/s0304-3940(96)13254-7.
71. Summers, C. H., Forster, G. L., Korzan, W. J., Watt, M. J., Larson, E., Overli, O., et al. (2005a). Dynamics and mechanics of social rank reversal. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 241-252. doi: 10.1007/s00359- 004-0554-z
72. Summers, T. R., Matter, J. M., Mckay, J. M., Ronan, P. J., Larson, E. T., Renner, K. J., et al. (2003). Rapid glucocorticoid stimulation and GABAergic inhibition of hippocampal serotonergic response: in vivo dialysis in the lizard Anolis carolinensis. Horm. Behav. 43, 245-253. doi: 10.1016/s0018-506x(02)00014-4.
73. Summers, T. R., Summers, T. L., Carpenter, R. E., Smith, J. P., Arendt, D. H., and Summers, C. H. (2011). Plasticity resulting from aggression induced social choice in Rainbowtrout. Soc. Neurosci. Abst. 37:943-919.
74. Summers, C. H., Watt, M. J., Ling, T. J., Forster, G. L., Carpenter, R. E., Korzan, W. J., et al. (2005b). Glucocorticoid interaction with aggression in nonmammalian vertebrates: reciprocal action. Eur. J. Pharmacol. 526, 21-35. doi: 10. 1016/j.ejphar.2005.09.059.
75. Takahashi, L. K., Ho, S. P., Livanov, V., Graciani, N., and Arneric, S. P. (2001). Antagonism of CRF 2 receptors produces anxiolytic behavior in animal models ofanxiety. Brain Res. 902, 135-142. doi: 10.1016/s0006-8993(01)02405-2.
76. Tanaka, K., Furuyashiki, T., Kitaoka, S., Senzai, Y., Imoto, Y., Segi-Nishida, E., et al. (2012). Prostaglandin E2-mediated attenuation of mesocortical dopaminergic pathway is critical for susceptibility to repeated social defeat stress in mice. J. Neurosci. 32, 4319-4329. doi: 10.1523/JNEUROSCI.5952-11.2012.
77. Tasan, R. O., Nguyen, N. K., Weger, S., Sartori, S. B., Singewald, N., Heilbronn, R., et al. (2010). The central and basolateral amygdala are critical sites of neuropeptide Y/Y2 receptor-mediated regulation of anxiety and depression. J. Neurosci. 30, 6282-6290. doi: 10.1523/JNEUROSCI.0430-10.2010.
78. Taylor, S. L., Stanek, L. M., Ressler, K. J., and Huhman, K. L. (2011). Differential brain-derived neurotrophic factor expression in limbic brain regions following social defeat of territorial aggression. Behav. Neurosci. 125, 911-920. doi: 10. 1037/a0026172
79. Toth, I., and Neumann, I. D. (2013). Animal models of social avoidance and social fear. Cell Tissue Res. 354, 107-118. doi: 10.1007/s00441-013-1636-4.
80. Wegener, G., Finger, B. C., Elfving, B., Keller, K., Liebenberg, N., Fischer, C. W., et al. (2012). Neuropeptide S alters anxiety, but not depression-like behaviour in flinders sensitive line rats: a genetic animal model of depression. Int. J. Neuropsychopharmacol. 15, 375-387. doi: 10.1017/S1461145711000678.
81. Xu, Y. L., Gall, C. M., Jackson, V. R., Civelli, O., and Reinscheid, R. K. (2007). Distribution of neuropeptide S receptor mRNA and neurochemical characteristics of neuropeptide S-expressing neurons in the rat brain. J. Comp. Neurol. 500, 84-102. doi: 10.1002/cne.21159.
82. Xu, Y. L., Reinscheid, R. K., Huitron-Resendiz, S., Clark, S. D., Wang, Z., Lin, S. H., et al. (2004). Neuropeptide S: a neuropeptide promoting arousal and anxiolyticlike effects. Neuron 43, 487-497. doi: 10.1016/j.neuron.2004.08.005.
83. Young, L. J. (2002). The neurobiology of social recognition, approach and avoidance. Biol. Psychiatry 51, 18-26. doi: 10.1016/s0006-3223(01)01268-9