The neurological ecology of fear: Insights neuroscientists and ecologists have to offer one another

Frontiers in Behavioral Neuroscience

Volumn , Issue APRIL, 2011, Pages

  Clinchy, Michael ^a   Schulkin, Jay ^b   Zanette, Liana Y ^c   Sheriff, Michael J ^d   McGowan, Patrick O ^e   Boonstra, Rudy ^e  

^a UNIVERSITY OF VICTORIA   (Canada)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Animal model of PTSD; Indirect predator effects; Post traumatic stress disorder; Predation risk; Predator stress

Indexed keywords

GLUCOCORTICOID;

ARTICLE; AUDITORY STIMULATION; CORTICOSTEROID BLOOD LEVEL; DENDRITE; DNA METHYLATION; FEAR; GENE EXPRESSION PROFILING; HUMAN; MENTAL STRESS; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOGENE C FOS; POSTTRAUMATIC STRESS DISORDER; PREDATOR STRESS; SUICIDE;

EID: 84855213297     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00021     Document Type: Article

References (58)

1. Adamec, R. E., and Shallow, T. (1993). Lasting effects on rodent anxiety of a single exposure to a cat. Physiol. Behav. 54, 101-109.
2. Armario, A., Escorihuela, R. M., and Nadal, R. (2008). Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci. Biobehav. Rev. 32, 1121-1135.
3. Blanchard, R. J., and Blanchard, D. C. (1989). Antipredator defensive behaviors in a visible burrow system. J. Comp. Psychol. 103, 70-82.
4. Blanchard, R. J., Nikulina, J. N., Sakai, R. R., McKittrick, C., McEwen, B., and Blanchard, D. C. (1998). Behavioral and endocrine change following chronic predatory stress. Physiol. Behav. 63, 561-569.
5. Boonstra, R., Hik, D., Singleton, G. R., and Tinnikov, A. (1998). The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 68, 371-394.
6. Calisi, R. M., and Bentley, G. E. (2009). Lab and field experiments: are they the same animal? Horm. Behav. 56, 1-10
7. Campeau, S., Nyhuis, T. J., Sasse, S. K., Day, H. E. W., and Masini, C. V. (2008). Acute and chronic effects of ferret odor exposure in SpragueDawley rats. Neurosci. Biobehav. Rev. 32, 1277-1286.
8. Cantor, C. (2009). Post-traumatic stress disorder: evolutionary perspectives. Aust. N. Z. J. Psychiatry 43, 1038-1048
9. Caro, T. M. (2005). Anti-Predator Defenses in Birds and Mammals. Chicago: University of Chicago Press.
10. Champagne, F. A., and Curley, J. P. (2009). Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci. Biobehav. Rev. 33, 593-600.
11. Chen, W., Tenney, J., Kulkarni, P., and King, J. A. (2007). Imaging unconditioned fear response with manganeseenhanced MRI (MEMRI). Neuroimage 37, 221-229.
12. Choi, J.-S., and Kim, J. J. (2010). Amygdala regulates risk of predation in rats foraging in a dynamic fear environment. Proc. Natl. Acad. Sci. U.S.A. 107, 21773-21777.
13. Clinchy, M., Zanette, L., Boonstra, R., Wingfield, J. C., and Smith, J. N. M. (2004). Balancing food and predator pressure induces chronic stress in songbirds. Proc. R. Soc. Lond. B Biol. Sci. 271, 2473-2479.
14. Clinchy, M., Zanette, L., Charlier, T. D., Newman, A. E. M., Schmidt, K. L., Boonstra, R., and Soma, K. K. (2011). Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat. Oecologia. doi: 10.1007/s00442-011-1915-2. [Epub ahead of print].
15. Cohen, H., Kozlovsky, N., Richter-Levin, G., and Zohar, J. (2010). "Posttraumatic stress disorder in animal models," in Stress From Molecules to Behaviour, eds H. Soreq, A. Friedman, and D. Kaufer (Weinheim: WileyVCH Verlag GmbH & Co. KGaA), 263-282.
16. Cohen, H., Matar, M. A., Richter-Levin, G., and Zohar, J. (2006). The contribution of an animal model toward uncovering biological risk factors for PTSD. Ann. N. Y. Acad. Sci. 1071, 335-350.
17. Creel, S., and Christianson, D. (2008). Relationships between direct predation and risk effects. Trends Ecol. Evol. 23, 194-201.
18. Creel, S., Winnie, J. A. Jr., and Christianson, D. (2009). Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proc. Natl. Acad. Sci. U.S.A. 106, 12388-12393.
19. Dielenberg, R. A., Hunt, G. E., and McGregor, I. S. (2001). 'When a rat smells a cat': the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104, 1085-1097.
20. Eggers, S., Griesser, M., Nystrand, M., and Ekman, J. (2006). Predation risk induces changes in nest-site selection and clutch size in the Siberian jay. Proc. R. Soc. Lond. B Biol. Sci. 273, 701-706
21. Febo, M., Shields, J., Ferris, C. F., and King, J. A. (2009). Oxytocin modulates unconditioned fear response in lactating dams: an fMRI study. Brain Res. 1302, 183-193.
22. Fontaine, J. J., and Martin, T. E. (2006). Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol. Lett. 9, 428-434.
23. Hawlena, D., and Schmitz, O. J. (2010). Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am. Nat. 176, 537-556.
24. Huang, W., Heffernan, M. E., Zhixin, L., Zhang, N., Overstreet, D. H., and King, J. A. (2011). Fear induced neuronal alterations in a genetic model of depression: an fMRI study on awake animals. Neurosci. Lett. 489, 74-78.
25. Jarvis, E. D. (2004). Learned birdsong and the neurobiology of human language. Ann. N. Y. Acad. Sci. 1016, 749-777
26. Jöngren, M., Westander, J., Nätt, D., and Jensen, P. (2010). Brain gene expression in relation to fearfulness in female red junglefowl (Gallus gallus). Genes Brain Behav. 9, 751-758.
27. Kappeler, L., and Meaney, M. J. (2010). Epigenetics and parental effects. Bioessays 32, 818-827.
28. Karels, T. J., Byrom, A. E., Boonstra, R., and Krebs, C. J. (2000). The interactive effects of food and predators on reproduction and overwinter survival of arctic ground squirrels. J. Anim. Ecol. 69, 235-247.
29. King, J. A., Garelick, T. S., Brevard, M. E., Chen, W., Messenger, T. L., Duong, T. Q., and Ferris, C. F. (2005). Procedure for minimizing stress for fMRI studies in conscious rats. J. Neurosci. Methods 148, 154-160.
30. Kotler, B. P. (1992). Behavioral resource depression and decaying perceived risk of predation in two species of coexisting gerbils. Behav. Ecol. Sociobiol. 30, 239-244.
31. Lupien, S. J., McEwen, B. S., Gunnar, M. R., and Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10, 434-445.
32. Mackenzie, L., Nalivaiko, E., Beig, M. I., Day, T. A., and Walker F. R. (2010). Ability of predator odor exposure to elicit conditioned versus sensitised post traumatic stress disorderlike behaviours, and forebrain FosB expression, in rats. Neuroscience 169, 733-742.
33. Masini, C. V., Sasse, S. K., Garcia, R. J., Nyhuis, T. J., Day, H. E. W., and Campeau, S. (2009). Disruption of neuroendocrine stress responses to acute ferret odor by medial, but not central amygdala lesions in rats. Brain Res. 1288, 79-87.
34. McClung, C. A., Ulery, P. G., Perrotti, L. I., Zachariou, V., Berton, O., and Nestler, E. J. (2004). FosB: a molecular switch for long-term adaptation in the brain. Mol. Brain Res. 132, 146-154.
35. McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., and Meaney, M. J. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12, 342-348.
36. McGowan, P. O., Sasaki, A., Huang, T. C. T., Unterberger, A., Suderman, M., Ernst, C., Meaney, M. J., Turecki, G., and Szyf, M. (2008). Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS ONE 3, e2085 doi: 10.1371/journal.pone.0002085
37. Mitra, R., Adamec, R., and Sapolsky, R. (2009). Resilience against predator stress and dendritic morphology of amygdala neurons. Behav. Brain Res. 205, 535-543.
38. Mitra, R., and Sapolsky, R. (2008). Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 105, 5573-5578.
39. Nanda, S. A., Qi, C., Roseboom, P. H., and Kalin, N. H. (2008). Predator stress induces behavioral inhibition and amygdala somatostatin receptor 2 gene expression. Genes Brain Behav. 7, 639-648.
40. Pilsner, J. R., Lazarus, A. L., Nam, D.-H., Letcher, R. J., Sonne, C., Dietz, R., and Basu, N. (2010). Mercury-associated DNA hypomethylation in polar bear brains via the LUminometric Methylation Assay: a sensitive method to study epigenetics in wildlife. Mol. Ecol. 19, 307-314.
41. Rodrigues, S. M., LeDoux, J. E., and Sapolsky, R. M. (2009). The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 32, 289-313.
42. Roseboom, P. H., Nanda, S. A., Bakshi, V. P., Trentani, A., Newman, S. M., and Kalin, N. H. (2007). Predator threat induces behavioral inhibition, pituitaryadrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 32, 44-55.
43. Rosen, J. B., Pagani, J. H., Rolla, K. L., and Davis, C. (2008). Analysis of behavioral constraints and the neuroanatomy of fear to the predator odor trimethylthiazoline: a model for animal phobias. Neurosci. Biobehav. Rev. 32, 1267-1276.
44. Rosen, J. B., and Schulkin, J. (1998). From normal fear to pathological anxiety. Psychol. Rev. 105, 325-350.
45. Schulkin, J. (2003). Rethinking Homeostasis. Cambridge, MA: MIT Press.
46. Schulkin, J., Morgan, M. A., and Rosen, J. B. (2005). A neuroendocrine mechanism for sustaining fear. Trends Neurosci. 28, 629-635.
47. Sheriff, M. J., Krebs, C. J., and Boonstra, R. (2009). The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J. Anim. Ecol. 78, 1249-1258.
48. Sheriff, M. J., Krebs, C. J., and Boonstra, R. (2010). The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91, 2983-2994.
49. Silva, A. C., Hee Lee, J., Aoki, I., and Koretsky, A. P. (2004). Manganeseenhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 17, 532-543. doi: 10.1002/ nbm.945
50. Stam, R. (2007). PTSD and stress sensitisation: a tale of brain and body. Part 2: animal models. Neurosci. Biobehav. Rev. 31, 558-584.
51. Stankowich, T., and Blumstein, D. T. (2005). Fear in animals: a meta- analysis and review of risk assessment. Proc. R. Soc. Lond. B Biol. Sci. 272, 2627-2634.
52. Staples, L. G., McGregor, I. S., and Hunt, G. E. (2009). Long-lasting FosB/ΔFosB immunoreactivity in the rat brain after repeated cat odor exposure. Neurosci. Lett. 462, 157-161.
53. Takahashi, L. K., Chan, M. M., and Pilar, M. L. (2008). Predator odor fear conditioning: current perspectives and new directions. Neurosci. Biobehav. Rev. 32, 1218-1227.
54. Travers, M., Clinchy, M., Zanette, L., Boonstra, R., and Williams, T. D. (2010). Indirect predator effects on clutch size and the cost of egg production. Ecol. Lett. 13, 980-988.
55. Van der Linden, A., Van Camp, N., Ramos-Cabrer, P., and Hoen, M. (2007). Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition. NMR Biomed. 20, 522-545. doi: 10.1002/nbm.1131
56. Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., and Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854.
57. Yehuda, R., and Bierer, L. M. (2009). The relevance of epigenetics to PTSD: implications for the DSM-V. J. Trauma. Stress 22, 427-434.
58. Zoumakis, E., Rice, K. C., Gold, P. W., and Chrousos, G. P. (2006). Potential uses of corticotropin-releasing hormone antagonists. Ann. N. Y. Acad. Sci. 1083, 239-251.