Relations between peripheral and brain serotonin measures and behavioural responses in a novelty test in pigs

Physiology and Behavior

Volumn 118, Issue , 2013, Pages 88-96

  Ursinus, Winanda W ^a   Bolhuis, J Elizabeth ^a   Zonderland, Johan J ^a,b   Rodenburg, T Bas ^a   de Souza, Adriana S ^a   Koopmanschap, Rudie E ^a   Kemp, Bas ^a   Korte Bouws, Gerdien A H ^c   Korte, S Mechiel ^c   van Reenen, Cornelis G ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Veterinary Health Research NZ   (New Zealand)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Behaviour; Blood; Brain; Novelty; Pigs; Serotonin

Indexed keywords

SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL TRAIT; CELL LEVEL; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEAR; FRONTAL CORTEX; HIPPOCAMPUS; HYPOTHALAMUS; METABOLITE; NONHUMAN; OBJECT RELATION; PRIORITY JOURNAL; PSYCHOLOGIC TEST; SEROTONIN BLOOD LEVEL; SEROTONIN BRAIN LEVEL; SEROTONIN METABOLISM; SEROTONIN UPTAKE; SEROTONINERGIC SYSTEM; SWINE; THROMBOCYTE;

EID: 84878836267     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.05.018     Document Type: Article

References (107)

1. Bracke M.B.M., Spruijt B.M., Metz J.H.M. Overall animal welfare reviewed. Part 3: welfare assessment based on needs and supported by expert opinion. Neth J Agr Sci 1999, 47:307-322.
2. Bracke M.B.M. RICHPIG: a semantic model to assess enrichment materials for pigs. Anim Welfare 2008, 17:289-304.
3. Beattie V.E., Breuer K., O'Connell N.E., Sneddon I.A., Mercer J.T., Rance K.A., et al. Factors identifying pigs predisposed to tail biting. Anim Sci 2005, 80:307-312.
4. Edwards S.A. Tail biting in pigs: understanding the intractable problem. Vet J 2006, 171:198-199.
5. Prunier A., Heinonen M., Quesnel H. High physiological demands in intensively raised pigs: impact on health and welfare. Animal 2010, 4:886-898.
6. Gentry J.G., McGlone J.J., Blanton J.R., Miller M.F. Alternative housing systems for pigs: Influences on growth, composition, and pork quality. J Anim Sci 2002, 80:1781-1790.
7. Bolhuis J.E., Schouten W.G.P., Schrama J.W., Wiegant V.M. Effects of rearing and housing environment on behaviour and performance of pigs with different coping characteristics. Appl Anim Behav Sci 2006, 101:68-85.
8. Van de Weerd H.A., Docking C.M., Day J.E.L., Breuer K., Edwards S.A. Effects of species-relevant environmental enrichment on the behaviour and productivity of finishing pigs. Appl Anim Behav Sci 2006, 99:230-247.
9. Zonderland J.J., Wolthuis-Fillerup M., van Reenen C.G., Bracke M.B.M., Kemp B., den Hartog L.A., et al. Prevention and treatment of tail biting in weaned piglets. Appl Anim Behav Sci 2008, 110:269-281.
10. Munsterhjelm C., Peltoniemi O.A.T., Heinonen M., Hälli O., Karhapää M., Valros A. Experience of moderate bedding affects behaviour of growing pigs. Appl Anim Behav Sci 2009, 118:42-53.
11. Koolhaas J.M., de Boer S.F., Coppens C.M., Buwalda B. Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 2010, 31:307-321.
12. Zupan M., Janczak A.M., Framstad T., Zanella A.J. The effect of biting tails and having tails bitten in pigs. Physiol Behav 2012, 106:638-644.
13. Van Hierden Y.M., Korte S.M., Ruesink E.W., Van Reenen C.G., Engel B., Korte-Bouws G.A.H., et al. Adrenocortical reactivity and central serotonin and dopamine turnover in young chicks from a high and low feather-pecking line of laying hens. Physiol Behav 2002, 75:653-659.
14. Bolhuis J.E., Ellen E.D., Van Reenen C.G., De Groot J., Napel J.T., Koopmanschap R.E., et al. Effects of genetic group selection against mortality on behavior and peripheral serotonin in domestic laying hens with trimmed and intact beaks. Physiol Behav 2009, 97:470-475.
15. Uitdehaag K.A., Rodenburg T.B., van Reenen C.G., Koopmanschap R.E., de Vries G.R., Engel B., et al. Effects of genetic origin and social environment on behavioral response to manual restraint and monoamine functioning in laying hens. Poult Sci 2011, 90:1629-1636.
16. Adeola O., Ball R.O., House J.D., O'Brien P.J. Regional brain neurotransmitter concentrations in stress-susceptible pigs. J Anim Sci 1993, 71:968-974.
17. Rosochacki S.J., Piekarzewska A.B., Połoszynowicz J., Sakowski T. Genetic differences in brain monoamines level in Pietrain and Duroc pigs exposed to acute restraint stress. J Anim Breed Genet 2003, 120:192-209.
18. Korpi E.R., Kleinman J.E., Goodman S.I. Serotonin and 5-hydroxyindoleacetic acid in brains of suicide victims. Comparison in chronic schizophrenic patients with suicide as cause of death. Arch Gen Psychiatry 1986, 43:594-600.
19. Parsey R.V., Oquendo M.A., Simpson N.R., Ogden R.T., Van Heertum R., Arango V., et al. Effects of sex, age, and aggressive traits in man on brain serotonin 5-HT 1A receptor binding potential measured by PET using [C-11]WAY-100635. Brain Res 2002, 954:173-182.
20. Barton D.A., Esler M.D., Dawood T., Lambert E.A., Haikerwal D., Brenchley C., et al. Elevated brain serotonin turnover in patients with depression: effect of genotype and therapy. Arch Gen Psychiatry 2008, 65:38-46.
21. Besiroglu L., Çetinkaya N., Selvi Y., Atli A. Effects of selective serotonin reuptake inhibitors on thought-action fusion, metacognitions, and thought suppression in obsessive-compulsive disorder. Compr Psychiatry 2011, 52:556-561.
22. Weiss J.M., Goodman P.A., Losito B.G. Behavioral depression produced by an uncontrollable stressor: relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain. Brain Res Rev 1981, 3:167-205.
23. Veenema A.H., Koolhaas J.M., De Kloet E.R. Basal and stress-induced differences in HPA axis, 5-HT responsiveness, and hippocampal cell proliferation in two mouse lines. Ann N Y Acad Sci 2004, 1018:255-265.
24. Caramaschi D., de Boer S.F., Koolhaas J.M. Differential role of the 5-HT1A receptor in aggressive and non-aggressive mice: an across-strain comparison. Physiol Behav 2007, 90:590-601.
25. Stahl S.M. The human platelet. A diagnostic and research tool for the study of biogenic amines in psychiatric and neurologic disorders. Arch Gen Psychiatry 1977, 34:509-516.
26. Chou D.T., Cuzzone H., Hirsh K.R. Assessment of blood platelets as a model for CNS response: comparative effects of caffeine on 5-HT uptake and release mechanisms in rat platelets and rat brain serotonin neurons. Life Sci 1983, 33:1149-1156.
27. Rausch J.L., Johnson M.E., Li J., Hutcheson J., Carr B.M., Corley K.M., et al. Serotonin transport kinetics correlated between human platelets and brain synaptosomes. Psychopharmacology 2005, 180:391-398.
28. Muck-Seler D., Pivac N. Serotonin. Period Biol 2011, 113:29-41.
29. Lesch K.P., Wolozin B.L., Murphy D.L., Riederer P. Primary structure of the human platelet serotonin uptake site: Identity with the brain serotonin transporter. J Neurochem 1993, 60:2319-2322.
30. Ostrowitzki S., Rao M.L., Redei J., Andres A.H. Concurrence of cortex and platelet serotonin2 receptor binding characteristics in the individual and the putative regulation by serotonin. J Neural Transm Gen Sect 1993, 93:27-35.
31. Bakish D., Cavazzoni P., Chudzik J., Ravindran A., Hrdina P.D. Effects of selective serotonin reuptake inhibitors on platelet serotonin parameters in major depressive disorder. Biol Psychiatry 1997, 41:184-190.
32. Askenazy F., Caci H., Myquel M., Darcourt G., Lecrubier Y. Relationship between impulsivity and platelet serotonin content in adolescents. Psychiatry Res 2000, 94:19-28.
33. Bianchi M., Moser C., Lazzarini C., Vecchiato E., Crespi F. Forced swimming test and fluoxetine treatment: In vivo evidence that peripheral 5-HT in rat platelet-rich plasma mirrors cerebral extracellular 5-HT levels, whilst 5-HT in isolated platelets mirrors neuronal 5-HT changes. Exp Brain Res 2002, 143:191-197.
34. Uitdehaag K.A., Rodenburg T.B., van Hierden Y.M., Bolhuis J.E., Toscano M.J., Nicol C.J., et al. Effects of mixed housing of birds from two genetic lines of laying hens on open field and manual restraint responses. Behav Processes 2008, 79:13-18.
35. Inderbitzen H.M., Hope D.A. Relationship among adolescent reports of social anxiety, anxiety, and depressive symptoms. J Anxiety Disord 1995, 9:385-396.
36. Smulders D., Hautekiet V., Verbeke G., Geers R. Tail and ear biting lesions in pigs: an epidemiological study. Anim Welfare 2008, 17:61-69.
37. Hashimoto S., Inoue T., Koyama T. Effects of conditioned fear stress on serotonin neurotransmission and freezing behavior in rats. Eur J Pharmacol 1999, 378:23-30.
38. Korte S.M. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 2001, 25:117-142.
39. Oquendo M.A., Mann J.J. Neuroimaging findings in major depression, suicidal behavior and aggression. Clin Neurosci Res. 2001, 1:377-380.
40. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007.
41. Melotti L., Oostindjer M., Bolhuis J.E., Held S., Mendl M. Coping personality type and environmental enrichment affect aggression at weaning in pigs. Appl Anim Behav Sci 2011, 133:144-153.
42. Oostindjer M., van den Brand H., Kemp B., Bolhuis J.E. Effects of environmental enrichment and loose housing of lactating sows on piglet behaviour before and after weaning. Appl Anim Behav Sci 2011, 134:31-41.
43. Curzon G., Green A.R. Rapid method for the determination of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid in small regions of rat brain. Br J Pharmacol 1970, 39:653-655.
44. Kluge H., Bolle M., Reuter R., Werner S., Zahlten W., Prudlo J. Serotonin in platelets: comparative analyses using new enzyme immunoassay and HPLC test kits and the traditional fluorimetric procedure. LaboratoriumsMedizin 1999, 23:360-364.
45. Da Prada M., Picotti G.B. Content and subcellular localization of catecholamines and 5-hydroxytryptamine in human and animal blood platelets: monoamine distribution between platelets and plasma. Br J Pharmacol 1979, 65:653-662.
46. Celada P., Martín F., Artigas F. Effects of chronic treatment with dexfenfluramine on serotonin in rat blood, brain and lung tissue. Life Sci 1994, 55:1237-1243.
47. Pussard E., Guigueno N., Adam O., Giudicelli J.F. Validation of HPLC-amperometric detection to measure serotonin in plasma, platelets, whole blood, and urine. Clin Chem 1996, 42:1086-1091.
48. Butler J., O'Halloran A., Leonard B.E. The Galway Study of Panic Disorder II: changes in some peripheral markers of noradrenergic and serotonergic function in DSM III-R Panic Disorder. J Affect Disord 1992, 26:89-99.
49. Thies-Flechtner K., Weigel I., Muller-Oerlinghausen B. 5-HT uptake in platelets of lithium-treated patients with affective disorders and of healthy controls. Pharmacopsychiatry 1994, 27:4-6. [Supplement].
50. Franke L., Schewe H.J., Müller B., Campman V., Kitzrow W., Uebelhack R., et al. Serotonergic platelet variables in unmedicated patients suffering from major depression and healthy subjects: Relationship between 5HT content and 5HT uptake. Life Sci 2000, 67:301-315.
51. De Groot J., Kruijt L., Scholten J.W., Boersma W.J.A., Buist W.G., Engel B., et al. Age, gender and litter-related variation in T-lymphocyte cytokine production in young pigs. Immunology 2005, 115:495-505.
52. Félix B., Léger M.E., Albe-Fessard D., Marcilloux J.C., Rampin O., Laplace J.P., et al. Stereotaxic atlas of the pig brain. Brain Res Bull 1999, 49:1-138.
53. Barf T., Korte S.M., Korte-Bouws G., Sonesson C., Damsma G., Bohus B., et al. Potential anxiolytic properties of R-(+)-8-OSO2CF3-PAT, a 5-HT1A receptor agonist. Eur J Pharmacol 1996, 297:205-211.
54. Korte-Bouws G.A.H., Korte S.M., De Kloet E.R., Bohus B. Blockade of corticosterone synthesis reduces serotonin turnover in the dorsal hippocampus of the rat as measured by microdialysis. J Neuroendocrinol 1996, 8:877-881.
55. Jernej B., Banović M., Cicin-Šain L., Hranilović D., Balija M., Orešković D., et al. Physiological characteristics of platelet/circulatory serotonin: study on a large human population. Psychiatr Res 2000, 94:153-162.
56. Buckley M.F., James J.W., Brown D.E., Whyte G.S., Dean M.G., Chesterman C.N., et al. A novel approach to the assessment of variations in the human platelet count. Thromb Haemost 2000, 83:480-484.
57. Pietraszek M.H., Yan D., Urano T., Sakakibara K., Serizawa K., Takada Y., et al. Correlations between serotonin and related substances simultaneously obtained from rat brain and blood. Biog Amines 1992, 9:123-129.
58. Malyszko J., Urano T., Serizawa K., Yan D., Kozima Y., Takada Y., et al. Serotonergic measures in blood and brain and their correlations in rats treated with tranylcypromine, a monoamine oxidase inhibitor. Jpn J Physiol 1993, 43:613-626.
59. Pietraszek M.H., Takada Y., Yan D., Urano T., Serizawa K., Takada A. Relationship between serotonergic measures in periphery and the brain of mouse. Life Sci 1992, 51:75-82.
60. Yatham L.N., Steiner M., Liddle P.F., Shiah I.S., Lam R.W., Zis A.P., et al. A PET study of brain 5-HT2 receptors and their correlation with platelet 5-HT2 receptors in healthy humans. Psychopharmacology 2000, 151:424-427.
61. Ritvo E., Yuwiler A., Geller E., Plotkin S., Mason A., Saeger K. Maturational changes in blood serotonin levels and platelet counts. Biochem Med 1971, 5:90-96.
62. Yuwiler A., Brammer G.L., Morley J.E., Raleigh M.J., Flannery J.W., Geller E. Short-term and repetitive administration of oral tryptophan in normal men. Effects on blood tryptophan, serotonin, and kynurenine concentrations. Arch Gen Psychiatry 1981, 38:619-626.
63. Badcock N.R., Spence J.G., Stern L.M. Blood serotonin levels in adults, autistic and non-autistic children - with a comparison of different methodologies. Ann Clin Biochem 1987, 24:625-634.
64. Jernej B., Cicin-Sain L. Platelet serotonin level in rats is under genetic control. Psychiatry Res 1990, 32:167-174.
65. Pazos A., Hoyer D., Palacios J.M. Mesulergine, a selective serotonin-2 ligand in the rat cortex, does not label these receptors in porcine and human cortex: Evidence for species differences in brain serotonin-2 receptors. Eur J Pharmacol 1985, 106:531-538.
66. Wang C.C., Billett E., Borchert A., Kuhn H., Ufer C. Monoamine oxidases in development. Cell Mol Life Sci 2013, 70(4):599-630.
67. Berumen L.C., Rodríguez A., Miledi R., García-Alcocer G. Serotonin receptors in hippocampus. ScientificWorldJournal 2012, 2012:823493.
68. Smith L.T., Hanson D.R., Omenn G.S. Comparisons of serotonin uptake by blood platelets and brain synaptosomes. Brain Res 1978, 146:400-403.
69. Smith D.F., Hansen S.B., Østergaard L., Gee A.D., Danielsen E., Ishizu K., et al. [14C]Serotonin uptake and [O-methyl-11C]venlafaxine kinetics in porcine brain. Nucl Med Biol 2001, 28:633-638.
70. Sánchez C. R-citalopram attenuates anxiolytic effects of escitalopram in a rat ultrasonic vocalisation model. Eur J Pharmacol 2003, 464:155-158.
71. Thor K.B. Targeting serotonin and norepinephrine receptors in stress urinary incontinence. Int J Gynecol Obstet 2004, 86:S38-S52.
72. Song G.H., Gwee K.A., Moochhala S.M., Ho K.Y. Melatonin attenuates stress-induced defecation: lesson from a rat model of stress-induced gut dysfunction. Neurogastroenterol Motil 2005, 17:744-750.
73. Andersen I.L., Bøe K.E., Foerevik G., Janczak A.M., Bakken M. Behavioural evaluation of methods for assessing fear responses in weaned pigs. Appl Anim Behav Sci 2000, 69:227-240.
74. Varty G.B., Morgan C.A., Cohen-Williams M.E., Coffin V.L., Carey G.J. The gerbil elevated plus-maze I: behavioral characterization and pharmacological validation. Neuropsychopharmacology 2002, 27:357-370.
75. Andersen I.L., Foerevik G., Bøe K.E., Janczak A.M., Bakken M. Effects of diazepam on the behaviour of weaned pigs in three putative models of anxiety. Appl Anim Behav Sci 2000, 68:121-130.
76. Lauber M.C., Hemsworth P.H., Barnett J.L. The effect of breed, time spent with dam and late pregnancy induction of parturition on behavioural development in dairy calves. Behav Process 2009, 82:301-311.
77. Cavigelli S.A., Michael K.C., West S.G., Klein L.C. Behavioral responses to physical vs. social novelty in male and female laboratory rats. Behav Process 2011, 88:56-59.
78. Lucki I. The spectrum of behaviors influenced by serotonin. Biol Psychiatry 1998, 44:151-162.
79. Désiré L., Veissier I., Després G., Boissy A. On the way to assess emotions in animals: do lambs (Ovis aries) evaluate an event through its suddenness, novelty, or unpredictability?. J Comp Psychol 2004, 118:363-374.
80. Forkman B., Boissy A., Meunier-Salaün M.C., Canali E., Jones R. B. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol Behav 2007, 92:340-374.
81. Korte S.M., de Boer S.F. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur J Pharmacol 2003, 463:163-175.
82. Brennan M.J., Dallob A., Friedman E. Involvement of hippocampal serotonergic activity in age-related changes in exploratory behaviour. Neurobiol Aging 1981, 2:199-203.
83. Campbell B.M., Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 2003, 993:1-9.
84. Reimert I., Bolhuis J.E., Kemp B., Rodenburg T.B. Indicators of positive and negative emotions and emotional contagion in pigs. Physiol Behav 2013, 109:42-50.
85. Vicens-Costa E., Martínez-Membrives E., López-Aumatell R., Guitart-Masip M., Cañete T., Blázquez G., et al. Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: a dissection of anxiety and fear in genetically heterogeneous rats. Physiol Behav 2011, 103:148-156.
86. Antoniadis E.A., McDonald R.J. Amygdala, hippocampus and discriminative fear conditioning to context. Behav Brain Res 2000, 108:1-19.
87. Benetti F., De Araujo P.A., Sanvitto G.L., Lucion A.B. Effects of neonatal novelty exposure on sexual behavior, fear, and stress-response in adult rats. Dev Psychobiol 2007, 49:258-264.
88. Campler M., Jöngren M., Jensen P. Fearfulness in red junglefowl and domesticated White Leghorn chickens. Behav Process 2009, 81:39-43.
89. Vanderwolf C.H. A general role for serotonin in the control of behavior: studies with intracerebral 5,7-dihydroxytryptamine. Brain Res 1989, 504:192-198.
90. Hessing M.J.C., Hagelsø A.M., van Beek J.A.M., Wiepkema R.P., Schouten W.G.P., Krukow R. Individual behavioural characteristics in pigs. Appl Anim Behav Sci 1993, 37:285-295.
91. Van Reenen C.G., Engel B., Ruis-Heutinck L.F.M., Van Der Werf J.T.N., Buist W.G., Jones R.B., et al. Behavioural reactivity of heifer calves in potentially alarming test situations: a multivariate and correlational analysis. Appl Anim Behav Sci 2004, 85:11-30.
92. Hansenne M., Pitchot W., Ansseau M. Serotonin, personality and borderline personality disorder. Acta Neuropsychiatr 2002, 14:66-70.
93. Boissy A. Fear and fearfulness in animals. Q Rev Biol 1995, 70:165-191.
94. Stanley W.C., Jaynes J. The function of the frontal cortex. Psychol Rev 1949, 56:18-32.
95. Colpaert F.C. The ventromedial hypothalamus and the control of avoidance behavior and aggression: fear hypothesis versus response suppression theory of limbic system function. Behav Biol 1975, 15:27-44.
96. Olton D.S., Wenk G.L., Church R.M., Meck W.H. Attention and the frontal cortex as examined by simultaneous temporal processing. Neuropsychologia 1988, 26:307-318.
97. Kruk M.R., Westphal K.G.C., Van Erp A.M.M., van Asperen J., Cave B.J., Slater E., et al. The hypothalamus: cross-roads of endocrine and behavioural regulation in grooming and aggression. Neurosci Biobehav R. 1998, 23:163-177.
98. Dayan P., Huys Q.J.M. Serotonin in affective control. Annu Rev Neurosci 2009, 32:95-126.
99. Antoniadis E.A., McDonald R.J. Amygdala, hippocampus, and unconditioned fear. Exp Brain Res 2001, 138:200-209.
100. Van der Staay F.J., Schuurman T., van Reenen C.G., Korte S.M. Emotional reactivity and cognitive performance in aversively motivated tasks: a comparison between four rat strains. Behav Brain Funct 2009, 5.
101. Dos Santos L., De Andrade T.G., Graeff F.G. Social separation and diazepam withdrawal increase anxiety in the elevated plus-maze and serotonin turnover in the median raphe and hippocampus. J Psychopharmacol 2010, 24:725-731.
102. Andrade R., Beck S.G. Cellular effects of serotonin in the CNS. Handbook of the behavioural neurobiology of serotonin 2010, 219-231. Academic Press, London. C.R. Müller, B. Jacobs (Eds.).
103. Carlson J.N., Glick S.D. Cerebral lateralization as a source of interindividual differences in behavior. Experientia 1989, 45:788-798.
104. Delrue C., Deleplanque B., Rougepont F., Vitiello S., Neveu P.J. Brain monoaminergic, neuroendocrine, and immune responses to an immune challenge in relation to brain and behavioral lateralization. Brain Behav Immun 1994, 8:137-152.
105. Hecht D. Depression and the hyperactive right-hemisphere. Neurosci Res 2010, 68:77-87.
106. Rogers L.J. Relevance of brain and behavioural lateralization to animal welfare. Appl Anim Behav Sci 2010, 127:1-11.
107. Fitzgerald P.J. Whose side are you on: does serotonin preferentially activate the right hemisphere and norepinephrine the left?. Med Hypotheses 2012, 79:250-254.