Stress During Adolescence Shapes Performance in Adulthood: Context-Dependent Effects on Foraging and Vigilance

Ethology

Volumn 122, Issue 4, 2016, Pages 284-297

  Chaby, Lauren E ^a,b   Sheriff, Michael J ^a   Cavigelli, Sonia A ^a,b   Hirrlinger, Amy M ^a   Lim, James ^a   Braithwaite, Victoria A ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Adolescence; Chronic stress; Foraging; Laboratory rodent; Risk; Risk sensitive

Indexed keywords

ADOLESCENCE; ADULT; COGNITION; FORAGING EFFICIENCY; PERFORMANCE ASSESSMENT; PHYSIOLOGICAL RESPONSE; RISK ASSESSMENT; RISK FACTOR; RODENT; TIME ALLOCATION; VIGILANCE;

ANIMALIA; RATTUS; RODENTIA;

EID: 84959483985     PISSN: 01791613     EISSN: 14390310     Source Type: Journal    
DOI: 10.1111/eth.12463     Document Type: Article

References (98)

1. Adamec, R. E. & Shallow, T. 1993: Lasting effects on rodent anxiety of a single exposure to a cat. Physiol. Behav. 54, 101-109.
2. Anderson, R. M., Shanmuganayagam, D. & Weindruch, R. 2009: Caloric restriction and aging: studies in mice and monkeys. Toxicol. Pathol. 37, 47-51.
3. Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A. & McGregor, I. S. 2005: The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29, 1123-1144.
4. Arditi, R. & Dacorogna, B. 1988: Optimal foraging on arbitrary food distributions and the definition of habitat patches. Am. Nat. 131, 837-846.
5. Bachman, G. C. 1993: The effect of body condition on the trade-off between vigilance and foraging in Belding's ground squirrels. Anim. Behav. 46, 233-244.
6. Bhatnagar, S., Vining, C., Iyer, V. & Kinni, V. 2006: Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J. Neuroendocrinol. 18, 13-24.
7. Blanchard, R. J., Mast, M. & Blanchard, D. C. 1975: Stimulus control of defensive reactions in the albino rat. J. Comp. Physiol. Psychol. 88, 81-88.
8. Blumstein, D. T. 1996: How much does social group size influence golden marmot vigilance? Behaviour 133, 1133-1151.
9. Blumstein, D. T., Daniel, J. C. & Springett, B. P. 2004: A test of the multi-predator hypothesis: rapid loss of antipredator behavior after 130 years of isolation. Ethology 110, 919-934.
10. Borgen, F. H. & Seling, M. J. 1978: Uses of discriminant analysis following MANOVA: multivariate statistics for multivariate purposes. J. Appl. Psychol. 63, 689.
11. Breuner, C. 2008: Maternal stress, glucocorticoids, and the maternal/fetal match hypothesis. Horm. Behav. 54, 485-487.
12. Bronstein, P. M. & Hirsch, S. M. 1976: Ontogeny of defensive reactions in Norway rats. J. Comp. Physiol. Psychol. 90, 620-629.
13. Brown, J. S. 1999: Vigilance, patch use and habitat selection: foraging under predation risk. Evol. Ecol. Res. 1, 49-71.
14. Brown, J. S., Laundré, J. W. & Gurung, M. 1999: The ecology of fear: optimal foraging, game theory, and trophic interactions. J. Mammal. 80, 385-399.
15. Bueno, C. H., Zangrossi, H. Jr & Viana, M. B. 2005: The inactivation of the basolateral nucleus of the rat amygdala has an anxiolytic effect in the elevated T-maze and light/dark transition tests. Braz. J. Med. Biol. Res. 38, 1697-1701.
16. Buwalda, B., Stubbendorff, C., Zickert, N. & Koolhaas, J. M. 2013: Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience 249, 258-270.
17. Byrne, A. & Eysenck, M. W. 1995: Trait anxiety, anxious mood, and threat detection. Cogn. Emot. 9, 549-562.
18. Candland, D. K. & Nagy, Z. M. 1969: The open field: some comparative data. Ann. N. Y. Acad. Sci. 159, 831-851.
19. Caruso, M. J., McClintock, M. K. & Cavigelli, S. A. 2014: Temperament moderates the influence of periadolescent social experience on behavior and adrenocortical activity in adult male rats. Horm. Behav. 66, 517-524.
20. Chaby, L. E., Cavigelli, S. A., White, A., Wang, K. & Braithwaite, V. A. 2013: Long-term changes in cognitive bias and coping response as a result of chronic unpredictable stress during adolescence. Front. Hum. Neurosci. 7, 328.
21. Chaby, L. E., Cavigelli, S. A., Hirrlinger, A. M., Caruso, M. J. & Braithwaite, V. A. 2014: Chronic unpredictable stress during adolescence causes long-term anxiety. Behav. Brain Res. 278, 492-495.
22. Chaby, L. E., Sheriff, M. J., Hirrlinger, A. M. & Braithwaite, V. A. 2015a: Does early stress prepare individuals for a stressful future? Stress during adolescence improves foraging under threat. Anim. Behav. 105, 37-45.
23. Chaby, L. E., Sheriff, M. J., Hirrlinger, A. M. & Braithwaite, V. A. 2015b: Can we understand how developmental stress enhances performance under future threat with the Yerkes-Dodson law? Commun. Integr. Biol. 8, e1029689.
24. Clarke, J. A. 1983: Moonlight's influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behav. Ecol. Sociobiol. 13, 205-209.
25. Clinchy, M., Schulkin, J., Sheriff, M. J., McGowan, P. O. & Boonstra, R. 2011: The neurological ecology of fear: insights neuroscientists and ecologists have to offer one another. Front. Behav. Neurosci. 5, 21.
26. Crone, E. A. & Dahl, R. E. 2012: Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat. Rev. Neurosci. 13, 636-650.
27. Crozier, W. J. & Pincus, G. 1927: Phototropism in young rats. J. Gen. Physiol. 10, 407-417.
28. Davis, M. 1990: Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect. Pharmacol. Ther. 47, 147-165.
29. Doyle, R. E., Lee, C., Deiss, V., Fisher, A. D., Hinch, G. N. & Boissy, A. 2011: Measuring judgement bias and emotional reactivity in sheep following long-term exposure to unpredictable and aversive events. Physiol. Behav. 102, 503-510.
30. Eilam, D., Dayan, T., Ben-Eliyahu, S., Schulman, I. I., Shefer, G. & Hendrie, C. A. 1999: Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim. Behav. 58, 1085-1093.
31. Favreau, F. R., Goldizen, A. W., Fritz, H., Blomberg, S. P., Best, E. C. & Pays, O. 2014: Within-population differences in personality and plasticity in the trade-off between vigilance and foraging in kangaroos. Anim. Behav. 92, 175-184.
32. Fendt, M. & Endres, T. 2008: 2, 3, 5-Trimethyl-3-thiazoline (TMT), a component of fox odor - just repugnant or really fear-inducing? Neurosci. Biobehav. Rev. 32, 1259-1266.
33. Field, A. 2013: Discovering Statistics Using IBM SPSS Statistics, 4th edn. Sage Publications Ltd, London, UK.
34. Ford, R. G. 1983: Home range in a patchy environment: optimal foraging predictions. Am. Zool. 23, 315-326.
35. Gluckman, P. D., Hanson, M. A. & Spencer, H. G. 2005: Predictive adaptive responses and human evolution. Trends Ecol. Evol. 20, 527-533.
36. Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. F., Herman, D. H., Clasen, L. S., Toga, A. W., Rapoport, J. L. & Thompson, P. M. 2004: Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 101, 8174-8179.
37. Graham, L. K., Yoon, T. & Kim, J. J. 2010: Stress impairs optimal behavior in a water foraging choice task in rats. Learn. Mem. 17, 1-4.
38. Green, M. R., Barnes, B. & McCormick, C. M. 2013: Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long-Evans rats. Dev. Psychobiol. 55, 849-859.
39. Grønli, J., Murison, R., Fiske, E., Bjorvatn, B., Sørensen, E., Portas, C. M. & Ursin, R. 2005: Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84, 571-577.
40. Han, X., Wang, W., Xue, X., Shao, F. & Li, N. 2011: Brief social isolation in early adolescence affects reversal learning and forebrain BDNF expression in adult rats. Brain Res. Bull. 86, 173-178.
41. Harding, E. J., Paul, E. S. & Mendl, M. 2004: Animal behaviour: cognitive bias and affective state. Nature 427, 312.
42. Harris, A. P., D'Eath, R. B. & Healy, S. D. 2009: Environmental enrichment enhances spatial cognition in rats by reducing thigmotaxis (wall hugging) during testing. Anim. Behav. 77, 1459-1464.
43. Isgor, C., Kabbaj, M., Akil, H. & Watson, S. J. 2004: Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14, 636-648.
44. Kabbaj, M., Isgor, C., Watson, S. J. & Akil, H. 2002: Stress during adolescence alters behavioral sensitization to amphetamine. Neuroscience 113, 395-400.
45. Kaviani, H., Gray, J. A., Checkley, S. A., Raven, P. W., Wilson, G. D. & Kumari, V. 2004: Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety. J. Affect. Disord. 83, 21-31.
46. Keagy, J., Savard, J. F. & Borgia, G. 2009: Male satin bowerbird problem-solving ability predicts mating success. Anim. Behav. 78, 809-817.
47. Keenan, K. P., Smith, P. F., Hertzog, P., Soper, K., Ballam, G. C. & Clark, R. L. 1994: The effects of overfeeding and dietary restriction on Sprague-Dawley rat survival and early pathology biomarkers of aging. Toxicol. Pathol. 22, 300-315.
48. Keller, F. S. 1941: Light-aversion in the white rat. Psychol. Rec. 4, 235-250.
49. Kendig, M. D., Bowen, M. T., Kemp, A. H. & McGregor, I. S. 2011: Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience. Behav. Brain Res. 225, 405-414.
50. Klaassen, R. H. G., Nolet, B. A. & Van Leeuwen, C. H. A. 2007: Prior knowledge about spatial pattern affects patch assessment rather than movement between patches in tactile-feeding mallard. J. Anim. Ecol. 76, 20-29.
51. Kotler, B. P. 1984: Risk of predation and the structure of desert rodent communities. Ecology 65, 689-701.
52. Kotler, B. P., Brown, J. S. & Bouskila, A. 2004: Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 85, 917-922.
53. Lima, S. L. & Bednekoff, P. A. 1999: Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am. Nat. 153, 649-659.
54. Lima, S. L. & Dill, L. M. 1990: Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640.
55. MacLeod, C. & Mathews, A. 1988: Anxiety and the allocation of attention to threat. Q. J. Exp. Psychol. A 40, 653-670.
56. MacLeod, C., Mathews, A. & Tata, P. 1986: Attentional bias in emotional disorders. J. Abnorm. Psychol. 95, 15-20.
57. Maren, S. 2001: Neurobiology of Pavlovian Fear Conditioning. Annual Review of Neuroscience 24, 897-931.
58. Mathew, R. J., Ho, B. T., Kralik, P., Taylor, D. L. & Claghorn, J. L. 1981: Catecholamines and monoamine oxidase activity in anxiety. Acta Psychiatr. Scand. 63, 245-252.
59. McCormick, C. M. & Mathews, I. Z. 2010: Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 756-765.
60. McCormick, C. M., Smith, C. & Mathews, I. Z. 2008: Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav. Brain Res. 187, 228-238.
61. McCormick, C. M., Mathews, I. Z., Thomas, C. & Waters, P. 2010: Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn. 72, 73-85.
62. McCormick, C. M., Thomas, C. M., Sheridan, C. S., Nixon, F., Flynn, J. A. & Mathews, I. Z. 2012: Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22, 1300-1312.
63. Melzig, C. A., Michalowski, J. M., Holtz, K. & Hamm, A. O. 2008: Anticipation of interoceptive threat in highly anxiety sensitive persons. Behav. Res. Ther. 46, 1126-1134.
64. Merali, Z., Levac, C. & Anisman, H. 2003: Validation of a simple, ethologically relevant paradigm for assessing anxiety in mice. Biol. Psychiatry 54, 552-565.
65. Morris, D. W. & Davidson, D. L. 2000: Optimally foraging mice match patch use with habitat differences in fitness. Ecology 81, 2061-2066.
66. Moskowitz, G. B. 2005: Social Cognition: Understanding Self and Others. Guilford Press, New York, NY. 417 pp.
67. Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Lucassen, P. J., Krugers, H. 2010: Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 30, 6635-6645.
68. Ottoni, E. B. 2000: EthoLog 2.2 - a tool for the transcription and timing of behavior observation sessions. Behav. Res. Methods Instrum. Comput. 32, 446-449.
69. Pare, W. P. 1965: Stress and consummatory behavior in the albino rat. Psychol. Rep. 16, 399-405.
70. Pearl, J., Walters, G. C. & Chris, D. 1964: Suppressing effects of aversive stimulation on subsequently punished behaviour. Can. J. Psychol. 18, 343-355.
71. Pietrelli, A., Lopez-Costa, J., Goñi, R., Brusco, A. & Basso, N. 2012: Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats. Neuroscience 202, 252-266.
72. Putman, B. J. & Clark, R. W. 2015: The fear of unseen predators: ground squirrel tail flagging in the absence of snakes signals vigilance. Behav. Ecol. 26, 185-193.
73. Quenette, P. Y. 1990: Functions of vigilance behaviour in mammals: a review. Acta Oecol. 11, 801-818.
74. Ribeiro-Barbosa, E. R., Canteras, N. S., Cezário, A. F., Blanchard, R. J. & Blanchard, D. C. 2005: An alternative experimental procedure for studying predator-related defensive responses. Neurosci. Biobehav. Rev. 29, 1255-1263.
75. Richardson, B. D., Ling, L. L., Uteshev, V. V. & Caspary, D. M. 2013: Reduced GABAA receptor-mediated tonic inhibition in aged rat auditory thalamus. J. Neurosci. 33, 1218-1227.
76. Romeo, R. D. 2010: Pubertal maturation and programming of hypothalamic-pituitary-adrenal reactivity. Front. Neuroendocrinol. 31, 232-240.
77. Romeo, R. D. & McEwen, B. 2006: Stress and the adolescent brain. Ann. N. Y. Acad. Sci. 1094, 202-214.
78. Samuels, B. A. & Hen, R. 2011: Novelty-suppressed feeding in the mouse. In: Mood and Anxiety Related Phenotypes in Mice, Vol. 63 (Gould, T. D., Ed.). Humana Press, Totowa, pp. 107-121.
79. Schmidt, M. V., Sterlemann, V., Ganea, K., Liebl, C., Alam, S., Harbich, D., Greetfeld, M., Uhr, M., Holsboer, F., Müller, M. B. 2007: Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32, 417-429.
80. Seamans, J. K., Floresco, S. B. & Phillips, A. G. 1995: Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav. Neurosci. 109, 1063-1073.
81. Sevy, S., Papadimitriou, G. N., Surmont, D. W., Goldman, S. & Mendiewicz, J. 1989: Noradrenergic function in generalized anxiety disorder, major depressive disorder, and healthy subjects. Biol. Psychiatry 25, 141-152.
82. Shechner, T., Britton, J. C., Pérez-Edgar, K., Bar-Haim, Y., Ernst, M., Fox, N. A., Leibenluft, E., Pine, D. S. 2012: Attention biases, anxiety, and development: toward or away from threats or rewards?. Depress. Anxiety 29, 282-294.
83. Sheriff, M. J. 2015: The adaptive potential of maternal stress exposure in regulating population dynamics. J. Anim. Ecol. 84, 323-325.
84. Sheriff, M. J. & Love, O. P. 2013: Determining the adaptive potential of maternal stress. Ecol. Lett. 16, 271-280.
85. Shimizu, N., Oomura, Y. & Kai, Y. 1989: Stress-induced anorexia in rats mediated by serotonergic mechanisms in the hypothalamus. Physiol. Behav. 46, 835-841.
86. Sih, A. & McCarthy, T. M. 2002: Prey responses to pulses of risk and safety: testing the risk allocation hypothesis. Anim. Behav. 63, 437-443.
87. Simon, P., Dupuis, R. & Costentin, J. 1994: Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav. Brain Res. 61, 59-64.
88. Snaith, T. V. & Chapman, C. A. 2005: Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behav. Ecol. Sociobiol. 59, 185-190.
89. Spear, L. P. 2000: The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24, 417-463.
90. Sterlemann, V., Rammes, G., Wolf, M., Liebl, C., Ganea, K., Müller, M. B. & Schmidt, M. V. 2010: Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20, 540-549.
91. Toledo-Rodriguez, M. & Sandi, C. 2011: Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats. Front. Behav. Neurosci. 5, 17.
92. Valone, T. J. & Brown, J. S. 1989: Measuring patch assessment abilities of desert granivores. Ecology 70, 1800-1810.
93. Van Eden, C. G., Kros, J. M. & Uylings, H. B. 1990: The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas. Prog. Brain Res. 85, 169-183.
94. Vásquez, R. A. 1997: Vigilance and social foraging in Octodon degus (Rodentia: Octodontidae) in central Chile. Rev. Chil. Hist. Nat. 70, 557-563.
95. Vásquez, R. A., Ebensperger, L. A. & Bozinovic, F. 2002: The influence of habitat on travel speed, intermittent locomotion, and vigilance in a diurnal rodent. Behav. Ecol. 13, 182-187.
96. Watson, R. T., Mathis, A. & Thompson, R. 2004: Influence of physical stress, distress cues, and predator kairomones on the foraging behavior of Ozark zigzag salamanders, Plethodon angusticlavius. Behav. Process. 65, 201-209.
97. Whishaw, I. Q. & Kolb, B. 2005: The Behavior of the Laboratory Rat: A Handbook with Tests. Oxford Univ. Press, New York, NY. 217 pp.
98. Whishaw, I. Q., Dringenberg, H. C. & Comery, T. A. 1992: Rats (Rattus norvegicus) modulate eating speed and vigilance to optimize food consumption: effects of cover, circadian rhythm, food deprivation, and individual differences. J. Comp. Psychol. 106, 411-419.