Predatory stress as an experimental strategy to measure fear and anxiety-related behaviors in non-human primates

Reviews in the Neurosciences

Volumn 19, Issue 2-3, 2008, Pages 157-169

  Barros, Marilia ^a,b   Maior, Rafael Souto ^b   Huston, Joseph P ^c   Tomaz, Carlos ^a,b  

^a School of Health Sciences   (Brazil)

^b UNIVERSITY OF BRASILIA   (Brazil)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Anti predation behavior; Anxiety; Diazepam; Marmoset; Predatory stress; Serotonin; Substance; Wild cat

Indexed keywords

BUSPIRONE; DIAZEPAM; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SUBSTANCE P [1-7];

ANXIETY; AVOIDANCE BEHAVIOR; CAT; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL TEST; FEAR; HABITUATION; MARMOSET; MARMOSET PREDATOR CONFRONTATION TEST; NONHUMAN; PREDATION RISK; PRIORITY JOURNAL; REVIEW; STRESS; VALIDATION STUDY;

EID: 48849097784     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2008.19.2-3.157     Document Type: Review

References (89)

1. Barros M, Boere V, Huston JP, Tomaz C. Measuring fear and anxiety in the marmoset (Callithrix penicillata) with a novel predator confrontation model: effects of diazepam. Behav Brain Res 2000; 108: 205-211.
2. Barros M, Mello EL, Huston JP, Tomaz C. Behavioral effects of buspirone in the marmoset employing a predator confrontation test of fear and anxiety. Pharmacol Biochem Behav 2001; 68: 255-262.
3. Barros M, Boere V, Mello EL, Tomaz C. Reactions to potential predators in captive-bom marmosets (Callithrix penicillata). Int J Primatol 2002; 23: 443-454.
4. 1-7) in non-human primates (Callithrix penicillata). Peptides 2002; 23: 967-973.
5. Barros M, Tomaz C. Non-human primate models for investigating fear and anxiety. Neurosci Biobehav Rev 2002; 26: 187-201.
6. 1A receptor antagonist WAY 100635 in non-human primates. Eur J Pharmacol 2003; 482: 197-203.
7. Barros M, Alencar C, Tomaz C. Differences in aerial and terrestrial visual scanning in captive black tufted-ear marmosets (Callithrix penicillata) exposed to a novel environment. Folia Primatol 2004; 75: 85-92.
8. Barros M, de Souza Silva MA, Huston JP, Tomaz C. Multibehavioral analysis of fear and anxiety before, during, and after experimentally induced predatory stress in Callithrix penicillata. Pharmacol Biochem Behav 2004; 78: 357-367.
9. Barros M, Giorgetti M, Souto AA, Vilela G, Santos K, Boas NV, Tomaz C. Persistent anxiety-like behavior in marmosets following a recent predatory stress condition: reversal by diazepam. Pharmacol Biochem Behav 2007; 86: 705-711.
10. Bartecki U, Heymann EW. Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons. Folia Primatol 1987; 48: 199-202.
11. Blanchard DC, Griebel G, Rodgers RJ, Blanchard RJ. Benzodiazepine and serotonergic modulation of antipredator and conspecific defense. Neurosci Biobehav Rev 1998; 22: 597-612.
12. Blanchard DC, Griebel G, Blanchard RJ. Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27: 1177-1185.
13. Blanchard RJ, Blanchard DC. Antipredator defensive behaviors in a visible burrow system. J Comp Psychol 1989; 103: 70-82.
14. Blanchard RJ, Yudko EB, Rodgers RJ, Blanchard DC. Defense system psychopharmacology: an ethological approach to the pharmacology of fear and anxiety. Behav Brain Res 1993; 58: 155-165.
15. Blanchard RJ, Yang M, Li CI, Gervacio A, Blanchard DC. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neurosci Biobehav Rev 2001; 25: 587-595.
16. Buchanan-Smith HM. Exploration of unfamiliar areas and detection of potentially threatening objects in single- and mixed-species groups of tamarins. Int J Comp Psychol 1999; 12: 2-20.
17. Caine NG. Visual scanning by tamarins: a description of the behavior and tests of 2 derived hypotheses. Folia Primatol 1984; 43: 59-67.
18. Caine NG. Vigilance, vocalizations and cryptic behavior at retirement in captive groups of red-bellied tamarins (Saguinus labiatus). Am J Primatol 1987; 12: 241-250.
19. Caine NG, Marra SL. Vigilance and social organization in 2 species of primates. Anim Behav 1988; 36: 897-904.
20. Caine NG, Weldon PJ. Responses by red-bellied tamarins (Saguinus labiatus) to fecal scents of predatory and non-predatory neotropical mammals. Biotropica 1989;21: 186-189.
21. Caine NG. Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour, role of predation pressures. In: Rylands AB, ed. Marmosets and Tamarins: Systematics, Behaviour and Ecology. New York: Oxford University Press, 1993; 200-219.
22. Caine NG. Cutting costs in response to predatory threat by Geoffrey's marmosets (Callithrix geffroyi). Am J Primatol 1998;46: 187-196.
23. Cheney DL, Seyfarth RM, Smuts BB, Wrangham RW. The study of primate societies. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, eds. Primate Societies. Chicago, IL: Chicago University Press, 1987; 1-8.
24. Cheney DL, Wrangham RW. Predation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, eds. Primates. Chicago, IL: Chicago University Press, 1987; 227-239.
25. Cilia J, Piper DC. Marmoset conspecific confrontation: an ethologically-based model of anxiety. Pharmacol Biochem Behav 1997; 58: 85-91.
26. 1A receptor ligand E-4424 to inhibit aversive behavior in the mouse, rat and marmoset. J Pharmacol Exp Ther 1992; 262: 90-98.
27. Dacier A, Maia R, Agustinho DP, Barros M. Rapid habituation of scan behavior in captive marmosets following brief predator encounters. Behav Processes 2006; 71: 66-69.
28. Darwin C. The Expression of the Emotions in Man and Animals. Chicago, IL: University of Chicago Press, 1965.
29. Day RT, Elwood RW. Sleeping site selection by the golden-handed tamarin Saguinus midas midas: the role of predation risk, proximity to feeding sites and territorial defence. Ethology 1999; 105: 1035-1051.
30. Dettling AC. Early deprivation and behavioral and physiological responses to social separation/novelty in the marmoset. Pharmacol Biochem Behav 2002; 73: 259-269.
31. Dielenberg RA, Carrive P, McGregor IS. The cardiovascular and behavioral response to cat odor in rats: unconditioned and conditioned effects. Brain Res 2001; 897: 228-237.
32. Dielenberg RA, McGregor IS. Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 2001; 25: 597-609.
33. Diezinger F, Anderson JR. Starting from scratch: a first look at a displacement activity in group-living rhesus monkeys. Am J Primatol 1986; 11: 117-124.
34. Echeverry MB, Hasenohrl RU, Huston JP, Tomaz C. Comparison of neurokinin SP with diazepam in effects on memory and fear parameters in the elevated T-maze free exploration paradigm. Peptides 2001; 22: 1031-1036.
35. Emmons LH. Comparative feeding ecology of felids in a neotropical rain-forest. Behav Ecol Sociobiol 1987; 20: 271-283.
36. Epple G. Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatol 1968; 8: 1-40.
37. Epple G. The behavior of the marmoset monkeys (Callitrichidade). In: Rosemblum L, ed. Primate Behavior. New York: Academic Press, 1975; 195-239.
38. Erickson K, Gabry KE, Lindell S, Champoux M, Schulkin J, Gold P, Suomi SJ, Higley JD. Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Dev Psychobiol 2005; 46: 331-339.
39. Ferrari SF, Ferrari MAL. Predator avoidance behavior in the buffy-headed marmoset, Callithrix flaviceps. Primates 1990; 31:323-338.
40. 1A receptor antagonist. Behav Brain Res 1996; 73: 337-353.
41. 1A agonist effects on punished responding of squirrel monkeys. Pharmacol Biochem Behav 1990; 37: 335-337.
42. Goldizen AW. Tamarins and marmosets: communal care of offspring. In: Smutts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, eds. Primate Societies. Chicago, IL: University of Chicago Press, 1987; 34-43.
43. German JM. Treatment of generalized anxiety disorder. J Clin Psychiatry 2002; 63 (Suppl 8): 17-23.
44. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacol Ther 1995; 65: 319-395.
45. 1A receptor antagonists in three rat models of anxiety. Neuropharmacology 2000; 39: 1848-1857.
46. 1A receptor antagonist, has anxiogenic effects in rats and does not block stress-induced rises in stress hormones. Soc Neurosci Abst 1995; 21: 1366.
47. Hankerson SJ, Caine NG. Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi). Am J Primatol 2004; 63: 75-85.
48. Hardie SM, Buchanan-Smith HM. Vigilance in single-and mixed-species groups of tamarins (Saguinus labiatus and Saguinus fuscicollis). Int J Primatol 1997; 18: 217-234.
49. Hardie SM, Buchanan-Smith HM. Responses of captive single-and mixed-species groups of Saguinus to novel nonthreatening objects. Int J Primatol 2000; 21: 629-648.
50. Hasenohrl RU, Jentjens O, De Souza Silva MA, Tomaz C, Huston JP. Anxiolytic-like action of neurokinin substance P administered systemically or into the nucleus basalis magnocellularis region. Eur J Pharmacol 1998; 354: 123-133.
51. Hasenohrl RU, Souza-Silva MA, Nikolaus S, Tomaz C, Brandao ML, Schwarting RK, Huston JP. Substance P and its role in neural mechanisms governing learning, anxiety and functional recovery. Neuropeptides 2000; 34: 272-280.
52. Heymann EW. Reactions of wild tamarins, Saguinus mystax and Saguinus fuscicollis, to avian predators. Int J Primatol 1990; 11: 327-337.
53. Hook-Costigan MA, Rogers LJ. Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 1998; 36: 1265-1273.
54. Johnson EO, Kamilaris TC, Carter CS, Calogero AE, Gold PW, Chrousos GP. The biobehavioral consequences of psychogenic stress in a small, social primate (Callithrix jacchus jacchus). Biol Psychiatry 1996; 40: 317-337.
55. Kalin NH, Shelton SE, Davidson RJ, Kelley AE. The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. J Neurosci 2001; 21: 2067-2074.
56. Kalin NH, Shelton SE. Nonhuman primate models to study anxiety, emotion regulation, and psycho-pathology. Ann NY Acad Sci 2003; 1008: 189-200.
57. Kaplan G, Rogers LJ. Parental care in marmosets (Callithrix jacchus jacchus): development and effect of anogenital licking on exploration. J Comp Psychol 1999; 113: 269-276.
58. Kavaliers M, Choleris E. Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 2001; 25: 577-586.
59. King FA, Yarbrough CJ, Anderson DC, Gordon TP, Gould KG. Primates. Science 1988; 240: 1475-1482.
60. Koenig A. Visual scanning by common marmosets (Callithrix jacchus): functional aspects and the special role of adult males. Primates 1998; 39: 85-90.
61. Kramer MS, Cutler N, Feighner J, Shrivastava R, Carman J, Sramek JJ, Reines SA, Liu G, Snavely D, Wyatt-Knowles E, Hale JJ, Mills SG, MacCoss M, Swain CJ, Harrison T, Hill RG, Hefti F, Scolnick EM, Cascieri MA, Chicchi GG, Sadowski S, Williams AR, Hewson L, Smith D, Carlson EJ, Hargreaves RJ, Rupniak NM. Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science 1998; 281: 1640-1645.
62. Maestripieri D, Schino G, Aureli F, Troisi A. A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 1992; 44: 967-979.
63. Marks IM, Nesse RM. Fear and fitness: an evolutionary 247-261.
64. Nesse RM. Proximate and evolutionary studies of anxiety, stress and depression: synergy at the interface. Neurosci Biobehav Rev 1999; 23: 895-903.
65. Norcross JL, Newman JD. Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus). Am J Primatol 1999; 47: 209-222.
66. Passamani M. Field observation of a group of Geoffrey's marmosets mobbing a margay cat. Folia Primatol 1995; 64: 163-166.
67. Patel JB, Migler B. A sensitive and selective monkey conflict test. Pharmacol Biochem Behav 1982; 17: 645-649.
68. Peres CA. Anti-predation benefits in a mixed-species group of Amazonian tamarins. Folia Primatol 1993; 61: 61-76.
69. Radulovic J, Kammermeier J, Spiess J. Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition and unconditioned stimulus preexposure. J Neurosci 1998; 18: 7452-7461.
70. Rodgers RJ. Animal models of 'anxiety': where next? Behav Pharmacol 1997; 8: 477-496; discussion 497-504.
71. Rogers DC, Costall B, Domeney AM, Gerrard PA, Greener M, Kelly ME, Hagan JJ, Hunter AJ. Anxiolytic profile of ropinirole in the rat, mouse and common marmoset. Psychopharmacology 2000; 151: 91-97.
72. Rowlett JK, Lelas S, Tomatzky W, Licata SC. Anticonflict effects of benzodiazepines in rhesus monkeys: relationship with therapeutic doses in humans and role of GABAA receptors. Psychopharmacology 2006; 184: 201-211.
73. Rylands AB, Mittermeier RA, Rodriguez-Luna E. Conservation of neotropical primates: threatened species and an analysis of primate diversity by country and region. Folia Primatol 1997; 68: 134-160.
74. Savage A, Snowdon CT, Giraldo LH, Soto LH. Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus). In: Norconk MA, Rosenberger AL, Garber PA, eds. Adaptive Radiations of Neotropical Primates. New York: Plenum Press, 1996; 187-199.
75. Schino G, Perretta G, Taglioni AM, Monaco V, Troisi A. Primate displacement activities as an ethopharmacological model of anxiety. Anxiety 1996; 2: 186-191.
76. Searcy YM, Caine NG. Hawk calls elicit alarm and defensive reactions in captive Geoffrey's marmosets (Callithfix geoffroyi). Folia Primatol 2003; 74: 115-125.
77. Sepinwall J, Grodsky FS, Cook L. Conflict behavior in the squirrel monkey: effects of chlordiazepoxide, diazepam and JV-desmethyldiazepam. J Pharmacol Exp Ther 1978; 204: 88-102.
78. Smith AC, Kelez S, Buchanan-Smith HM. Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax). Behav Ecol Sociobiol 2004; 56: 18-25.
79. Smith TE, McGreer-Whitworth B, French JA. Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novelcage housing in black tufted-ear marmosets (Callithrix kuhli). Horm Behav 1998; 34: 211-222.
80. 1A receptor agonists, partial agonists and a silent antagonist on the performance of the conditioned emotional response test in the rat. Psychopharmacology 1996; 128: 293-303.
81. Stevenson MF, Poole TB. An ethogram of the commom marmoset (Callithrix jacchus jacchus): general behavioural repertoire. Anim Behav 1976; 24: 428-451.
82. Stevenson MF, Rylands AB. The marmosets, genus Callithrix. In: Mittermeier RA, Rylands AB, Coimbra-Filho A, Fonseca GAB, eds. Ecology and Behavior of Neotropical Primates. Contagem/Brazil: Littera Maciel Ltda./WWF, 1988; 131-222.
83. Sussman RW. Primate Ecology and Social Structure. Boston, MA: Pearson Custom Publishing, 2003.
84. Tello NS, Huck M, Heymann EW. Boa constrictor attack and successful group defence in moustached tamarins, Saguinus mystax. Folia Primatol 2002; 73: 146-148.
85. Tomaz C, Nogueira PJ. Facilitation of memory by peripheral administration of substance P. Behav Brain Res 1997; 83: 143-145.
86. Wettstein JG. Behavioral effects of acute and chronic buspirone. Eur J Pharmacol 1988; 151: 341-344.
87. Wettstein JG, Teeple ES, Morse WH. Respiratory effects of benzodiazepine-related drugs in awake rhesus monkeys. J Pharmacol Exp Ther 1990; 255: 1328-1334.
88. Winslow JT, Parr LA, Davis M. Acoustic startle, prepulse inhibition, and fear-potentiated startle measured in rhesus monkeys. Biol Psychiatry 2002; 51: 859-866.
89. Winslow JT, Noble PL, Davis M. Modulation of fearpotentiated startle and vocalizations in juvenile rhesus monkeys by morphine, diazepam, and buspirone. Biol Psychiatry 2007; 61: 389-395.