Journal of Veterinary Behavior: Clinical Applications and Research
Volume 7, Issue 1 , Pages 11-20 , January 2012

The effects of drug detection training on behavioral reactivity and blood neurotransmitter levels in drug detection dogs: A preliminary study

  • Jacopo Riva

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy
    • ,
  • Stefano P. Marelli

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy
    • Corresponding Author InformationAddress for reprint requests and correspondence: Stefano P. Marelli, PhD, Department of Animal Science, University of Milan, via Celoria, Medicine 10, 20133 Milan, Italy; Tel: +39-02-503-18028; Fax: +39-02-503-18030.
    • ,
  • Veronica Redaelli

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy
    • ,
  • Gianpietro P. Bondiolotti

      Affiliations

    • Department of Pharmacology, Chemotherapy and Toxicology, University of Milan, Milan, Italy
    • ,
  • Elisabetta Sforzini

      Affiliations

    • Med Vet, Libero professionista, Broni (PV), Italy
    • ,
  • Michele Matteo Santoro

      Affiliations

    • Guardia di Finanza, Servizio Cinofili, Castiglione del Lago (PG), Italy
    • ,
  • Corrado Carenzi

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy
    • ,
  • Marina Verga

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy
    • ,
  • Fabio Luzi

      Affiliations

    • Department of Animal Science, University of Milan, Milan, Italy

References 

  1. Aberg MAI, Pedersen NL, Toren K, Svartengren M, Backstrand B, Johnson T, et al. Cardiovascular fitness is associated with cognition in young adulthood. PNAS. 2009;106(49):20906–20911
  2. Acworth I, Nicholass J, Morgan B, Newsholme EA. Effects of sustained exercise on concentrations of plasma aromatic and branched-chain amino acids and brain amines. Biochem. Biophys. Res. Commun. 1986;137:149–153
  3. Alleva E, Cirulli F, Bianchi M, Bondiolotti GP, Chiarotti F, De Acetis L, et al. Behavioral characterization of interleukin-6 overexpressing or deficient mice during agonistic encounters. Eur. J. Neurosci. 1998;10:3664–3672
  4. Arvelius P, Malm S, Svartberg K, Strandberg E. Genetic analysis of herding behavior. In Sweedish Border Collie dogs. J. Vet. Behav.: Clin. Appl. Res. 2009;4:237
  5. Bailey SP, Davis JM, Ahlborn EN. Neuroendocrine and substrate responses to altered brain 5-HT activity during prolonged exercise to fatigue. J. Appl. Phys. 1993;74:3006–3012
  6. Batt SL, Batt MS, Baguley JA, McGreevy PD. The relationships between motor lateralization, salivary cortisol concentrations and behavior in dogs. J. Appl. Behav. 2009;4:216–222
  7. Beerda B, Schilder BH, Van Hoof JARAM, De Vries HW. Manifestations of chronic and acute stress in dogs. Appl. Anim. Behav. Sci. 1997;52:307–319
  8. Berquet F, Gomez-Merino D, Berthelot M, Guezennec CY. Evidence that brain glucose availability influences exercise-enhanced extracellular 5-HT level in hippocampus: a microdialysis study in exercising rats. Acta. Physiol. Scand. 2002;176:65–69
  9. Bondiolotti, G.P., Galva, M.D., Picotti, G.B., 1987. Simultaneous determination of catecholamines L-DOPA and DOPAC in human plasma by high performance liquid chromatography with electrochemical detection. In: Proceedings of 6th International Catecholamine Symposium, Jerusalem, Israel, June 14-19, p. 117.
  10. Bosch G, Beerda B, Hendriks WH, Van Der Poel AFB, Verstegen MWA. Impact of nutrition on canine behavior: current status and possible mechanisms. Nutr. Res. Rev. 2007;20:180–194
  11. Bradshaw JWS, Goodwin D. Determination of behavioral traits of pure-breed dogs using factor analysis; a comparison of studies in USA and UK. Res. Vet. Sci. 1999;66:73–76
  12. Bradshaw JWS, Goodwin D, Lea AM, Whitehead SL. A survey of the behavior characteristics of pure-breed dogs in the United Kingdom. Vet. Rec. 1996;138:465–468
  13. Broocks A, Meyer T, George A, Hillmer-Vogel U, Meyer D, Bandelow B, et al. Decreased neuroendocrine response to metachlorophenilpiperazine (m-CPP) but normal responses to ipsapirone in marathon runners. Neuropsychopharmacology. 1999;20:150–161
  14. Brown B, Payne T, Kim C, Moore G, Krebs P, Matin W. Chronic response of rat brain norepinephrine and serotonin levels to endurance training. J. Appl. Physiol. 1979;46:19–23
  15. Buhot MC, Martin S, Segu I. Role of serotonin in memory impairment. Ann. Med. 2000;32:210–221
  16. Chaouloff F. Physical exercise and brain monoamines: a review. Acta. Physiol. Scand. 1989;137:1–13
  17. Chaouloff F, Laude D, Guezennec Y, Elghozi JL. Motor activity increases tryptophan, 5-hydroxyindoleacetic acid, and homovanillic acid in ventricular cerebrospinal fluid of the conscious rat. J. Neurochem. 1986;46:1313–1316
  18. Chaouloff F, Laude D, Meringo D, Serrurrier B, Guezennec Y. Amphetamine and a - methyl-p-tyrosine affect the exercise induced imbalance between the availability of tryptophan and synthesis of serotonin in the brain of the rat. Neuropharmacology. 1987;26:1099–1106
  19. Coccaro EF, Kavoussi RJ, Sheline YI, Berman ME, Csernansky JG. Impulsive aggression in personality disorder correlates with platelet 5-HT2A receptor binding. Neuropsychopharmacology. 1997;16:211–216
  20. Cook EH, Fletcher KE, Wainwright M, Marks N, Yan SY, Leventhal BL. Primary structure of the human platelet serotonin 5-HT2A receptor: identify with frontal cortex serotonin 5-HT2A receptor. J. Neurochem. 1994;63:465–469
  21. Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25:295–301
  22. Da Prada M, Cesura AM, Launay JM, Richards JG. Platelets as a model for neurones?. Experientia. 1988;44:115–126
  23. Da Prada M, Picotti GB. 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
  24. Davis JM, Bailey SP. Possible mechanism of central nervous system fatigue during exercise. Med. Sci. Sports Exerc. 1997;29:45–57
  25. Dey S. Physical exercise as a novel antidepressant agent—possible role of serotonin receptor subtypes. Phys. Behav. 1994;55:323–329
  26. Dey S, Singh R, Dey K. Exercise training: significance of regional alterations in serotonin metabolism of rat brain in relation to antidepressant effect of exercise. Phys. Behav. 1992;52:1095–1099
  27. Diederich C, Giffroy JM. Temperament testing, from puppies to adulthood. J. Vet. Behav.: Clin. Appl. Res. 2009;4:237–238
  28. Diederich C, Verplancke G, Giffroy JM. Behavioral dog testing, how far from the field?. J. Vet. Behav.: Clin. Appl. Res. 2009;4:238
  29. Duffy DL, Hsu Y, Serpell JA. Breed differences in canine aggression. Appl. Anim. Behav. Sci. 2008;114:441–460
  30. Erikson L. The Swedish police system for selecting dogs for service. J. Vet. Behav.: Clin. Appl. Res. 2009;4:239
  31. Fernstrom JD, Wurtman RJ. Brain serotonin content: physiological dependence on plasma tryptophan levels. Science. 1971;173:149–152
  32. Gaines SA, Rooney NJ, Bradshaw JWS. The effect of feeding enrichment upon reported working ability and behavior of kenneled working dogs. J. Forensic Sci. 2008;53:1400–1404
  33. Gordon JL, Olverman HJ. 5-Hydroxytryptamine and dopamine transport by rat and human blood platelets. Br. J. Pharmacol. 1978;62:219–226
  34. Gosling SD, Hilliard SJ. Personality and performance in explosive-detection military working dogs (MWDS). J. Vet. Behav.: Clin. Appl. Res. 2009;4:239
  35. Haverbeke A, Diederich C, Depiereux E, Giffroy JM. Cortisol and behavioral responses of working dogs to environmental challenges. Physiol. Behav. 2008;93:59–67
  36. Haverbeke A, Laporte B, Depiereux E, Giffroy JM, Diederich C. Training methods of military dog handlers and their effects on team’s performances. Appl. Anim. Behav. Sci. 2008;113:110–122
  37. Hedlund PB. The 5-HT7 receptor and disorders of the nervous system: an overview. Psychopharmacology. 2009;206:345–354
  38. Herman JP, Cullinan WE. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 1997;20:78–84
  39. Hoffmann P, Elam M, Thoren P, Hjorth S. Effects of long-lasting voluntary running on cerebral levels of dopamine, serotonin and their metabolites in the spontaneously hypertensive rat. Life Sci. 1994;54:855–861
  40. Jakeman PM, Hawthorne JE, Maxwell SR, Kendall MJ, Holder G. Evidence for down regulation of hypothalamic 5-hydroxytriptamine receptor function in endurance-trained athletes. Exp. Physiol. 1994;79:461–464
  41. Jiansong Z, Lingjiang Li, Shaojun T, Xia C, Zexuan L, Weihui L, et al. Effects of serotonin depletion on the hippocampal GR/MR and BDNF expression during the stress adaptation. Behav. Brain Res. 2008;175:129–138
  42. King JN, Simpson BS, Overall KL, Appleby D, Pageat P, Ross C, et al. Treatment of separation anxiety in dogs with clomipramine: results from a prospective, randomized, double-blind, placebo-controlled, parallel-group, multicenter clinical trial. App. Anim. Behav. Sci. 2000;67:255–275
  43. Kubesch S, Bretschneider V, Freudenmann R, Weidenhammer N, Lehmann M, Spitzer M. Aerobic endurance exercise improves executive functions in depressed patients. J. Clin. Psych. 2003;64:1005–1012
  44. Kurosawa M, Okada K, Sato A, Uchida S. Extracellular release of acetylcholine, noradrenaline and serotonin increases in the cerebral cortex during walking in conscious rats. Neurosci. Lett. 1993;161:73–76
  45. Le Moal M, Simon H. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol. Rev. 1991;71:155–234
  46. Leighton EA. Secrets for producing high-quality working dogs. J. Vet. Behav.: Clin. Appl. Res. 2009;4:212–215
  47. Lollis C, Felten D, Shea P. HPLC determination of biogenic amines in discrete brain areas in food deprived rats. Pharmacol. Biochem. Behav. 1979;19:89–93
  48. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J. Biol. Chem. 1951;193:265–275
  49. Marelli, S.P., Riva, J., Sforzini, E., Stella, L., Di Mari, W., Luzi, F., Verga, M., 2008. Assessment of breed differences in German shepherd and Belgian malinois dog’s reactivity: a pilot study. In: Paul, K., the WAFL 2008 Scientific Committee, (Eds.) Book of abstracts of the 4th International Workshop on the Assessment of Animal Welfare at Farm and Group Level (WAFL), Gent, Belgium, p. 102.
  50. Marshal-Pescini S, Passalacqua C, Barnard S, Valsecchi P, Prato-previde E. Agility and search and rescue training differently affects pet dogs’ behavior in socio cognitive tasks. Behav. Proc. 2009;81:416–422
  51. Mazzeo R. Catecholamine responses to acute and chronic exercise. Med. Sci. Sports. Exerc. 1991;23:839–845
  52. Meeusen R, De Meirleir K. Exercise and brain neurotransmission. Sports Med. 1995;20:160–188
  53. Meeusen R, Piacentini MF, De Meirleir K. Brain mycodialysis in exercise research. Sports Med. 2001;31:965–983
  54. Meeusen R, Sarre S, Michotte Y, Ebinger G, De Meirleir K. The effects of exercise on neurotransmission in rat striatum, a microdialysis study. In:  Louilot A,  Durkin T,  Spampinato U,  Cador M editor. Monitoring Molecule in Neuroscience. Gardignan: Publy Typ; 1994;p. 181–182
  55. Meeusen R, Watson P, Hasegawa H, Roelands B, Piacentini MF. Central fatigue—the serotonin hypothesis and beyond. Sports Med. 2006;36:881–909
  56. Meeusen R, Watson P, Hasegawa H, Roelands B, Piacentini MF. Brain neurotransmitters in fatigue and overtraining. Appl. Physol. Nutr. Metab. 2007;32:857–864
  57. Mohammad-Zadeh LF, Moses L, Gwaltney-Brant SM. Serotonin: a review. J. Vet. Pharmacol. Ther. 2008;31:187–199
  58. Notari L, Goodwin D. A survey of behavioral characteristics of pure-breed dogs in Italy. Appl. Anim. Behav. Sci. 2007;103:1–2
  59. Ogren SO. Evidence for a role of brain serotoninergic neurotransmission in avoidance learning. Acta. Physiol. Scand. 1985;544:1–71
  60. Overall K, Dunham AE. Clinical features and outcome in dogs and cats with obsessive compulsive disorder: 126 cases (1989-2000). J. Am. Vet. Med. Assoc. 2002;221:1445–1452
  61. Overall KL, Dunham AE, Frank D. Frequency of nonspecific clinical signs in dogs with separation anxiety, thunderstorm phobia, and noise phobia, alone or in combination. J. Am. Vet. Med. Assoc. 2001;219:467–473
  62. Overall K, Juarbe-Diaz S, Dyer DJ, Chang ML, Yokoyama JS, Dunham AE. Assessing reactivity in three breeds of working dogs: phenotypic determination and associated genotypes. J. Vet. Behav.: Clin. Appl. Res. 2009;4:249
  63. Picotti GB, Bondiolotti GP, Cesura AM, Ravazzani C, Galva MD, Mantegazza P. Free (unconjugated) catecholamine concentrations in platelets: biological significance and clinical implications. Adv. Exp. Med. Biol. 1984;164:257–268
  64. Pletscher A. Metabolism, transfer and storage of 5-hydroxytryptamine in blood platelets. Br. J. Pharmacol. Chemother. 1968;32:1–16
  65. Puglisi-Allegra S, Cabib S. Effects of defeat experiences on dopamine metabolism in different brain areas of the mouse. Aggress. Behav. 1990;16:271–284
  66. Ramamoorthy S, Bauman AL, Moore KR, Han H, Yang-Feng T, Chang AS, et al. Antidepressant- and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization. Proc. Natl. Acad. Sci. 1993;90:2542–2546
  67. Reisner IR, Mann JJ, Stanley M, Huang YY, Houpt KA. Comparison of cerebrospinal fluid monoamine metabolite levels in dominant-aggressive and non-aggressive dogs. Brain Res. 1996;714:57–64
  68. Riva J, Bondiolotti G, Michelazzi M, Marelli SP, Luzi F, Verga M. Comparison of neurotransmitter levels and behaviors in drug detection dogs. J. Vet. Behav.: Clin. Appl. Res. 2007;2:86
  69. Riva J, Bondiolotti G, Michelazzi M, Verga M, Carenzi C. Anxiety related behavioral disorders and neurotransmitters in dogs. Appl. Anim. Behav. Sci. 2008;114:168–181
  70. Robertson DA, Beattie JE, Reid IC, Balfour DJ. Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress. Eur. J. Neurosci. 2005;21:1511–1520
  71. Roche BM, Schwartz D, Lehnhard RA, McKeever KH, Nakayama T, Kirby TE, et al. Changes in concentrations of neuroendocrine hormones and catecholamines in dogs with myocardial failure induced by rapid ventricular pacing. Am. J. Vet. Res. 2002;63:1413–1417
  72. Rooney N, Gaines S, Hiby E. A practitioner’s guide to working dog welfare. J. Vet. Behav.: Clin. Appl. Res. 2009;4:127–134
  73. Rooney NJ, Bradshaw JWS. Breed and sex differences in the behavioral attributes of specialist search dogs—a questionnaire survey of trainers and handlers. Appl. Anim. Behav. Sci. 2004;86:123–135
  74. Rooney NJ, Gaines SA, Bradshaw JWS, Penman S. Validation of a method for assessing the ability of trainee specialist search dogs. Appl. Anim. Behav. Sci. 2007;103:90–104
  75. Ruefenacht S, Gebhardt-Henrich S, Miyake T, Gaillard C. A behavior test on German shepherd dogs: heritability of seven different traits. Appl. Anim. Behav. Sci. 2002;79:113–132
  76. Sarrias MJ, Cabré P, Martínez E, Artigas F. Relationship between serotoninergic measures in blood and cerebrospinal fluid simultaneously obtained in humans. J. Neurochem. 1990;54:783–786
  77. SAS Institute. SAS® user’s guide: statistics. Cary, NC: SAS Institute Inc.; 2008;
  78. Seguin L, Liscia P, Guezennec Y, Fillion G. Effects of moderate and intensive training on functional activity of central 5-HT1B receptors in the rat substantia nigra. Acta. Physiol. Scand. 1998;162:63–68
  79. Seksel K, Lindeman MJ. Use of clomipramine in treatment of obsessive-compulsive disorder, separation anxiety and noise phobia in dogs: a preliminary, clinical study. Aust. Vet. J. 2001;79:252–256
  80. Shankaran H, Wiley HS, Resat H. Reception downregulation and desensitization enhance the information processing ability of signaling receptors. BMC Syst. Biol. 2007;1:48
  81. Stahl SM, Ciaranello RD, Berger PA. Platelet serotonin in schizophrenia and depression. Adv. Biochem. Psychopharmacol. 1982;34:183–198
  82. Svarberg K, Tapper I, Temrin H, Radesater T, Thorman S. Consistency of personality traits in dogs. Anim. Behav. 2005;69:283–291
  83. Svartberg K. A comparison of behavior in test and in everyday life: evidence of three consistent boldness-related personality traits in dogs. Appl. Anim. Behav. Sci. 2005;91:103–128
  84. Svartberg K. Breed typical behavior in dogs—historical remnants or recent construct?. Appl. Anim. Behav. Sci. 2006;96:293–313
  85. Svartberg K, Forkman B. Personality traits in the domestic dog (Canis familiaris). Appl. Anim. Behav. Sci. 2002;79:133–155
  86. Takeuchi Y, Mori Y. A comparison of behavioral profiles of purebred dogs in Japan to profiles of those in United States and in the United Kingdom. J. Vet. Med. Sci. 2006;68:789–796
  87. Taylor KD, Mills DS. The development and assessment of temperament tests for adult companion dogs. J. Vet. Behav.: Clin. Appl. Res. 2006;1:94–108
  88. Vanderloo J. The importance of integrating natural selection within a detector dog selective breeding model. J. Vet. Behav.: Clin. Appl. Res. 2009;4:245
  89. Wilson W, Marsden C. The effect of running on brain serotonin. In:  Louilot A,  Durkin T,  Spampinato U,  Cador M editor. Monitoring Molecule in Neuroscience. Gardignan: Publy Typ; 1994;p. 223–224
  90. Wilson WM, Maughan RJ. Evidence for a possible role of 5-hydroxytryptamine in the genesis of fatigue in man: administration of paroxetine, a 5-HT re-uptake inhibitor, reduces the capacity to perform prolonged exercise. Exp. Physiol. 1992;77:921–924
  91. Wilsson E. The kennel of the Swedish armed forces. J. Vet. Behav.: Clin. Appl. Res. 2009;4:248
  92. Yan D, Urano T, Pietraszek MH, Shimoyama I, Uemura K, Kojima Y, et al. Correlation between serotonergic measures in cerebrospinal fluid and blood of subhuman primate. Life Sci. 1993;52:745–749

PII: S1558-7878(11)00060-8

doi: 10.1016/j.jveb.2011.04.002

Journal of Veterinary Behavior: Clinical Applications and Research
Volume 7, Issue 1 , Pages 11-20 , January 2012

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