Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T17:01:08.306Z Has data issue: false hasContentIssue false

5 - Processes of Stress Resistance and Stress Resilience

The Role of Behavioral Control and the Medial Prefrontal Cortex

from Part I - Theoretical Perspectives on the Development of Coping

Published online by Cambridge University Press:  22 June 2023

By
Michael V. Baratta  and
Steven F. Maier
Edited by
Ellen A. Skinner  and
Melanie J. Zimmer-Gembeck
Ellen A. Skinner
Affiliation:
Portland State University
Melanie J. Zimmer-Gembeck
Affiliation:
Griffith University, Queensland
Get access

Summary

Coping strategies are important determinants of resilience, however it is often difficult to isolate such processes at the animal level where the underlying neurobiology can be explored. Here we review research indicating that the degree to which an organism can exert control over adverse events, a key element of coping, potently modulates the impact of the event, with uncontrollable stressors producing outcomes that do not occur if the stressor is controllable. The data suggest that the stress-resistance produced by control depends on activation of distinct neural systems involving the medial prefrontal cortex (mPFC). In addition, the experience of control changes how the mPFC responds to future adverse events, even those that are uncontrollable, thereby providing resilience that is both enduring and trans-situational. We also address sex differences within controllability phenomena, the extent to which other resilience-promoting factors engage similar circuitry, and the clinical implications of these findings.

Keywords

copingbehavioral controlresiliencestressmedial prefrontal cortexserotonin
Type
Chapter
Information
The Cambridge Handbook of the Development of Coping , pp. 128 - 154
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alloy, L., & Bersh, P. (1979). Partial control and learned helplessness in rats: Control over shock intensity prevents interference with subsequent escape. Learning & Behaviour, 7(2), 157–164. https://doi.org/10.3758/BF03209265Google Scholar
Amat, J., Aleksejev, R. M., Paul, E., Watkins, L. R., & Maier, S. F. (2010). Behavioral control over shock blocks behavioral and neurochemical effects of later social defeat. Neuroscience, 165(4), 1031–1038. https://doi.org/10.1016/j.neuroscience.2009.11.005Google Scholar
Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L. R., & Maier, S. F. (2005). Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neuroscience, 8(3), 365–371. https://doi.org/10.1038/nn1399Google Scholar
Amat, J., Christianson, J. P., Aleksejev, R. M., Kim, J., Richeson, K. R., Watkins, L. R., & Maier, S. F. (2014). Control over a stressor involves the posterior dorsal striatum and the act/outcome circuit. European Journal of Neuroscience, 40(3), 2352–2358. https://doi.org/10.1111/ejn.12609Google Scholar
Amat, J., Matus-Amat, P., Watkins, L. R., & Maier, S. F. (1998a). Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Research, 812(1–2), 113–120. https://doi.org/10.1016/s0006-8993(98)00960-3Google Scholar
Amat, J., Matus-Amat, P., Watkins, L. R., & Maier, S. F. (1998b). Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Research, 797(1), 12–22. https://doi.org/10.1016/S0006-8993(98)00368-0CrossRefGoogle ScholarPubMed
Amat, J., Paul, E., Watkins, L. R., & Maier, S. F. (2008). Activation of the ventral medial prefrontal cortex during an uncontrollable stressor reproduces both the immediate and long-term protective effects of behavioral control. Neuroscience, 154(4), 1178–1186. https://doi.org/10.1016/j.neuroscience.2008.04.005Google Scholar
Amat, J., Paul, E., Zarza, C., Watkins, L. R., & Maier, S. F. (2006). Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: Role of the ventral medial prefrontal cortex. Journal of Neuroscience, 26(51), 13264–13272. https://doi.org/10.1523/JNEUROSCI.3630-06.2006Google Scholar
Arnsten, A. F. (2015). Stress weakens prefrontal networks: Molecular insults to higher cognition. Nature Neuroscience, 18(3), 1376–1385. https://doi.org/10.1038/nn.4087CrossRefGoogle ScholarPubMed
Aspinwall, L. G. (2010). Future-oriented thinking, proactive coping, and the management of potential threats to health and well-being. In Folkman, S. (Ed.), The Oxford handbook of stress, health, and coping (pp. 334–365). Oxford University Press.Google Scholar
Balleine, B. W., & Dezfouli, A. (2019). Hierarchical action control: Adaptive collaboration between actions and habits. Frontiers in Psychology, 10, Article 2735. https://doi.org/10.3389/fpsyg.2019.02735CrossRefGoogle ScholarPubMed
Bandura, A. (1997). Self-efficacy: The exercise of control. Freeman.Google Scholar
Baratta, M. V., Christianson, J. P., Gomez, D. M., Zarza, C. M., Amat, J., Masini, C. V., Watkins, L. R., & Maier, S. F. (2007). Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear. Neuroscience, 146(4), 1495–1503. https://doi.org/10.1016/j.neuroscience.2007.03.042Google Scholar
Baratta, M. V., Gruene, T. M., Dolzani, S. D., Chun, L. E., Maier, S. F., & Shansky, R. M. (2019). Controllable stress elicits circuit-specific patterns of prefrontal plasticity in males, but not females. Brain Structure and Function, 224(5), 1831–1843. https://doi.org/10.1007/s00429-019-01875-zGoogle Scholar
Baratta, M. V., Leslie, N. R., Fallon, I. P., Dolzani, S. D., Chun, L. E., Tamalunas, A. M., Watkins, L. R., & Maier, S. F. (2018). Behavioural and neural sequelae of stressor exposure are not modulated by controllability in females. European Journal of Neuroscience, 47(8), 959–967. https://doi.org/10.1111/ejn.13833Google Scholar
Baratta, M. V., Lucero, T. R., Amat, J., Watkins, L. R., & Maier, S. F. (2008). Role of the ventral medial prefrontal cortex in mediating behavioral control-induced reduction of later conditioned fear. Learning and Memory, 15(2), 84–87. https://doi.org/10.1101/lm.800308Google Scholar
Baratta, M. V., & Maier, S. F. (2019). New tools for understanding coping and resilience. Neuroscience Letters, 693, 54–57. https://doi.org/10.1016/j.neulet.2017.09.049Google Scholar
Baratta, M. V., Zarza, C. M., Gomez, D. M., Campeau, S., Watkins, L. R., & Maier, S. F. (2009). Selective activation of dorsal raphe nucleus-projecting neurons in the ventral medial prefrontal cortex by controllable stress. European Journal of Neuroscience, 30(6), 1111–1116. https://doi.org/10.1111/j.1460-9568.2009.06867.xGoogle Scholar
Benjet, C., Bromet, E., Karam, E. G., Kessler, R. C., McLaughlin, K. A., Ruscio, A. M., … & Koenen, K. C. (2016). The epidemiology of traumatic event exposure worldwide: Results from the World Mental Health Survey Consortium. Psychological Medicine, 46(2), 327–343. https://doi.org/10.1017/S0033291715001981CrossRefGoogle ScholarPubMed
Bloodgood, D. W., Sugam, J. A., Holmes, A., & Kash, T. L. (2018). Fear extinction requires infralimbic cortex projections to the basolateral amygdala. Translational Psychiatry, 8(2), Article 60. https://doi.org/10.1038/s41398-018-0106-xGoogle Scholar
Bouton, M. E., Westbrook, R. F., Corcoran, K. A., & Maren, S. (2006). Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biological Psychiatry, 60(4), 352–360. https://doi.org/10.1016/j.biopsych.2005.12.015Google Scholar
Campbell, B. A., & Masterson, F. A. (1969). Psychophysics of punishment. In Campbell, B. A. & Church, R. M. (Eds.), Punishment and aversive behavior (pp. 3–42). Appleton-Century-Crofts.Google Scholar
Catania, A. C., & Sagvolden, T. (1980). Preference for free choice over forced choice in pigeons. Journal of the Experimental Analysis of Behavior, 34(1), 77–86. https://doi.org/10.1901/jeab.1980.34-77CrossRefGoogle ScholarPubMed
Cathomas, F., Murrough, J. W., Nestler, E. J., Han, M. H., & Russo, S. J. (2019). Neurobiology of resilience: Interface between mind and body. Biological Psychiatry, 86(6), 410–420. https://doi.org/10.1016/j.biopsych.2019.04.011Google Scholar
Christianson, J. P., Benison, A. M., Jennings, J., Sandsmark, E. K., Amat, J., Kaufman, R. D., Baratta, M. V., Paul, E. D., Campeau, S., Watkins, L. R., Barth, D. S., & Maier, S. F. (2008). The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. Journal of Neuroscience, 28(50), 13703–13711. https://doi.org/10.1523/JNEUROSCI.4270-08.2008Google Scholar
Christianson, J. P., Flyer-Adams, J. G., Drugan, R. C., Amat, J., Daut, R. A., Foilb, A. R., Watkins, L. R., & Maier, S. F. (2014). Learned stressor resistance requires extracellular signal-regulated kinase in the prefrontal cortex. Frontiers in Behavioral Neuroscience, 8, Article 348. https://doi.org/10.3389/fnbeh.2014.00348Google Scholar
Christianson, J. P., Jennings, J. H., Ragole, T., Flyer, J. G., Benison, A. M., Barth, D. S., Watkins, L. R., & Maier, S. F. (2011). Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis. Biological Psychiatry, 70(5), 458–464. https://doi.org/10.1016/j.biopsych.2011.04.004CrossRefGoogle Scholar
Christianson, J. P., Ragole, T., Amat, J., Greenwood, B. N., Strong, P. V., Paul, E. D., Fleshner, M., Watkins, L. R., & Maier, S. F. (2010). 5-hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biological Psychiatry, 67(4), 339–345. https://doi.org/10.1016/j.biopsych.2009.09.011Google Scholar
Cutuli, D. (2014). Cognitive reappraisal and expressive suppression strategies role in the emotion regulation: An overview on their modulatory effects and neural correlates. Frontiers in Systems Neuroscience, 8, Article 175.Google Scholar
Datta, D., Yang, S. T., Galvin, V. C., Solder, J., Luo, F., Morozov, Y. M., Arellano, J., Duque, A., Rakic, P., Arnsten, A. F. T., & Wang, M. (2019). Noradrenergic α1-adrenoceptor actions in the primate dorsolateral prefrontal cortex. Journal of Neuroscience, 39(14), 2722–2734. https://doi.org/10.1523/JNEUROSCI.2472-18.2019Google Scholar
de Kloet, E. R., de Kloet, S. F., de Kloet, C. S., & de Kloet, A. D. (2019). Top-down and bottom-up control of stress-coping. Journal of Neuroendocrinology, 31(3), 1–16. https://doi.org/10.1111/jne.12675Google Scholar
DeRubeis, R. J., Siegle, G. J., & Hollon, S. D. (2008). Cognitive therapy versus medication for depression: Treatment outcomes and neural mechanisms. Nature Reviews Neuroscience, 9(10), 788–796. https://doi.org/10.1038/nrn2345Google Scholar
Dezfouli, A., & Balleine, B. W. (2012). Habits, action sequences and reinforcement learning. European Journal of Neuroscience, 35(7), 1036–1051. https://doi.org/10.1111/j.1460-9568.2012.08050.xGoogle Scholar
Dickinson, A., & Balleine, B. W. (2000). Causal cognition and goal-directed action. In Heyes, C. & Huber, L. (Eds.), The evolution of cognition (pp. 185–204). The MIT Press.Google Scholar
Dolzani, S. D., Baratta, M. V., Amat, J., Agster, K. L., Saddoris, M. P., Watkins, L. R., & Maier, S. F. (2016). Activation of a Habenulo-Raphe circuit is critical for the behavioral and neurochemical consequences of uncontrollable stress in the male rat. eNeuro, 3(5). https://doi.org/10.1523/ENEURO.0229-16.2016Google Scholar
Drugan, R. C., Eren, S., Hazi, A., Silva, J., Christianson, J. P., & Kent, S. (2005). Impact of water temperature and stressor controllability on swim stress-induced changes in body temperature, serum corticosterone, and immobility in rats. Pharmacology, Biochemistry and Behavior, 82(2), 397–403. https://doi.org/10.1016/j.pbb.2005.09.011Google Scholar
Franklin, G., Carson, A. J., & Welch, K. A. (2016). Cognitive behavioural therapy for depression: Systematic review of imaging studies. Acta Neuropsychiatrica, 28(2), 61–74. https://doi.org/10.1017/neu.2015.41Google Scholar
Franklin, T. B. (2019). Recent advancements surrounding the role of the periaqueductal gray in predators and prey. Frontiers in Behavioral Neuroscience, 13, Article 60. https://doi.org/10.3389/fnbeh.2019.00060Google Scholar
Fredrickson, B. L., & Levenson, R. W. (1998). Positive emotions speed recovery from the cardiovascular sequelae of negative emotions. Cognition and Emotion, 12(2), 191–220. https://doi.org/10.1080/026999398379718Google Scholar
Giustino, T. F., & Maren, S. (2015). The role of the medial prefrontal cortex in the conditioning and extinction of fear. Frontiers in Behavioral Neuroscience, 9, Article 298.Google Scholar
Grahn, R. E., Hammack, S. E., Will, M. J., O’Connor, K. A., Deak, T., Sparks, P. D., Watkins, L. R., & Maier, S. F. (2002). Blockade of alpha1 adrenoreceptors in the dorsal raphe nucleus prevents enhanced conditioned fear and impaired escape performance following uncontrollable stressor exposure in rats. Behavioral Brain Research, 134(1–2), 387–392. https://doi.org/10.1016/S0166-4328(02)00061-XGoogle Scholar
Grahn, R. E., Watkins, L. R., & Maier, S. F. (2000). Impaired escape performance and enhanced conditioned fear in rats following exposure to an uncontrollable stressor are mediated by glutamate and nitric oxide in the dorsal raphe nucleus. Behavioral Brain Research, 112(1–2), 33–41. https://doi.org/10.1016/s0166-4328(00)00161-3Google Scholar
Grahn, R. E., Will, M. J., Hammack, S. E., Maswood, S., McQueen, M. B., Watkins, L. R., & Maier, S. F. (1999). Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Research, 826(1), 35–43. https://doi.org/10.1016/S0006-8993(99)01208-1Google Scholar
Greenwood, B. N., & Fleshner, M. (2019). Voluntary wheel running: A useful rodent model for investigating the mechanisms of stress robustness and neural circuits of exercise motivation. Current Opinion in Behavioral Sciences, 28, 78–84. https://doi.org/10.1016/j.cobeha.2019.02.001Google Scholar
Greenwood, B. N., Foley, T. E., Day, H. E., Campisi, J., Hammack, S. H., Campeau, S., Maier, S. F., & Fleshner, M. (2003). Freewheel running prevents learned helplessness/behavioral depression: Role of dorsal raphe serotonergic neurons. Journal of Neuroscience, 23(7), 2889–2898. https://doi.org/10.1523/JNEUROSCI.23-07-02889.2003Google Scholar
Greenwood, B. N., Spence, K. G., Crevling, D. M., Clark, P. J., Craig, W. C., & Fleshner, M. (2013). Exercise-induced stress resistance is independent of exercise controllability and the medial prefrontal cortex. European Journal of Neuroscience, 37(3), 469–478. https://doi.org/10.1111/ejn.12044Google Scholar
Hajós, M., Hajós-Korcsok, E., & Sharp, T. (1999). Role of the medial prefrontal cortex in 5-HT1A receptor-induced inhibition of 5-HT neuronal activity in the rat. British Journal of Pharmacology, 126(8), 1741–1750. https://doi.org/10.1038/sj.bjp.0702510Google Scholar
Hajós, M., Richards, C. D., Székely, A. D., & Sharp, T. (1998). An electrophysiological and neuroanatomical study of the medial prefrontal cortical projection to the midbrain raphe nuclei in the rat. Neuroscience, 87(1), 95–108. https://doi.org/10.1016/s0306-4522(98)00157-2Google Scholar
Hammack, S. E., Cooper, M. A., & Lezak, K. R. (2012). Overlapping neurobiology of learned helplessness and conditioned defeat: Implications for PTSD and mood disorders. Neuropharmacology, 62(2), 565–575. https://doi.org/10.1016/j.neuropharm.2011.02.024Google Scholar
Hammack, S. E., Richey, K. J., Schmid, M. J., LoPresti, M. L., Watkins, L. R., & Maier, S. F. (2002). The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. Journal of Neuroscience, 22(3), 1020–1026. https://doi.org/10.1523/JNEUROSCI.22-03-01020.2002Google Scholar
Hammack, S. E., Schmid, M. J., LoPresti, M. L., Der-Avakian, A., Pellymounter, M. A., Foster, A. C., Watkins, L. R., & Maier, S. F. (2003). Corticotropin releasing hormone type 2 receptors in the dorsal raphe nucleus mediate the behavioral consequences of uncontrollable stress. Journal of Neuroscience, 23(3), 1019–1025. https://doi.org/10.1523/JNEUROSCI.23-03-01019.2003Google Scholar
Hare, B. D., Beierle, J. A., Toufexis, D. J., Hammack, S. E., & Falls, W. A. (2014). Exercise-associated changes in the corticosterone response to acute restraint stress: Evidence for increased adrenal sensitivity and reduced corticosterone response duration. Neuropsychopharmacology, 39(5), 1262–1269. https://doi.org/10.1038/npp.2013.329Google Scholar
Hartogsveld, B., van Ruitenbeek, P., Quaedflieg, C., & Smeets, T. (2020). Balancing between goal-directed and habitual responding following acute stress. Experimental Psychology, 67(2), 99–111. https://doi.org/10.1027/1618-3169/a000485Google Scholar
Heinsbroek, R. P., van Haaren, F., Feenstra, M. G., Boon, P., & van de Poll, N. E. (1991). Controllable and uncontrollable footshock and monoaminergic activity in the frontal cortex of male and female rats. Brain Research, 551(1–2), 247–255. https://doi.org/10.1016/0006-8993(91)90939-sGoogle Scholar
Heinsbroek, R. P., van Haaren, F., Feenstra, M. G., Endert, E., & van de Poll, N. E. (1991). Sex- and time-dependent changes in neurochemical and hormonal variables induced by predictable and unpredictable footshock. Physiology & Behavior, 49(6), 1251–1256. https://doi.org/10.1016/0031-9384(91)90359-vCrossRefGoogle ScholarPubMed
Helmreich, D. L., Tylee, D., Christianson, J. P., Kubala, K. H., Govindarajan, S. T., O’Neill, W. E., Becoats, K., Watkins, L., & Maier, S. F. (2012). Active behavioral coping alters the behavioral but not the endocrine response to stress. Psychoneuroendocrinology, 37(12), 1941–1948. https://doi.org/10.1016/j.psyneuen.2012.04.005Google Scholar
Helmreich, D. L., Watkins, L. R., Deak, T., Maier, S. F., Akil, H., & Watson, S. J. (1999). The effect of stressor controllability on stress-induced neuropeptide mRNA expression within the paraventricular nucleus of the hypothalamus. Journal of Neuroendocrinology, 11(2), 121–128. https://doi.org/10.1046/j.1365-2826.1999.00300.xGoogle Scholar
Herman, J. P. (2018). Regulation of hypothalamo-pituitary-adrenocortical responses to stressors by the nucleus of the solitary tract/dorsal vagal complex. Cellular and Molecular Neurobiology, 38(1), 25–35. https://doi.org/10.1007/s10571-017-0543-8Google Scholar
Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010). Neuronal circuits of fear extinction. European Journal of Neuroscience, 31(4), 599–612. https://doi.org/10.1111/j.1460-9568.2010.07101.xGoogle Scholar
Hoover, W. B., & Vertes, R. P. (2007). Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Structure and Function, 212(2), 149–179. https://doi.org/10.1007/s00429-007-0150-4Google Scholar
Horn, S. R., Charney, D. S., & Feder, A. (2016). Understanding resilience: New approaches for preventing and treating PTSD. Experimental Neurology, 284, 119–132. https://doi.org/10.1016/j.expneurol.2016.07.002Google Scholar
Huang, X., Huang, P., Li, D., Zhang, Y., Wang, T., Mu, J., Li, Q., & Xie, P. (2014). Early brain changes associated with psychotherapy in major depressive disorder revealed by resting-state fMRI: Evidence for the top-down regulation theory. International Journal of Psychophysiology, 94(3), 437–444. https://doi.org/10.1016/j.ijpsycho.2014.10.011Google Scholar
Jankowski, M. P., & Sesack, S. R. (2004). Prefrontal cortical projections to the rat dorsal raphe nucleus: Ultrastructural features and associations with serotonin and gamma-aminobutyric acid neurons. Journal of Comparative Neurology, 468(4), 518–529. https://doi.org/10.1002/cne.10976Google Scholar
Johnson, S. B., Emmons, E. B., Lingg, R. T., Anderson, R. M., Romig-Martin, S. A., LaLumiere, R. T., Narayanan, N. S., Viau, V., & Radley, J. J. (2019). Prefrontal-bed nucleus circuit modulation of a passive coping response set. Journal of Neuroscience, 39(8), 1405–1419. https://doi.org/10.1523/JNEUROSCI.1421-18.2018Google Scholar
Kalisch, R., Müller, M. B., & Tüscher, O. (2015). A conceptual framework for the neurobiological study of resilience. Behavioral Brain Research, 38, e92. https://doi.org/10.1017/S0140525X1400082XGoogle Scholar
Kessler, R. C., Sonnega, A., Bromet, E., Hughes, M., & Nelson, C. B. (1995). Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry, 52(12), 1048–1060. https://doi.org/10.1001/archpsyc.1995.03950240066012Google Scholar
Kim, J. U., Weisenbach, S. L., & Zald, D. H. (2019). Ventral prefrontal cortex and emotion regulation in aging: A case for utilizing transcranial magnetic stimulation. International Journal of Geriatric Psychiatry, 34(2), 215–222. https://doi.org/10.1002/gps.4982Google Scholar
Kimura, M., Yamada, H., & Matsumoto, N. (2003). Tonically active neurons in the striatum encode motivational contexts of action. Brain Development, 25(Suppl. 1), S20–S23. https://doi.org/10.1016/s0387-7604(03)90003-9Google Scholar
Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C., Ruis, M. A., & Blokhuis, H. J. (1999). Coping styles in animals: Current status in behavior and stress-physiology. Neuroscience & Biobehavioral Reviews, 23(7), 925–935. https://doi.org/10.1016/s0149-7634(99)00026-3Google Scholar
Kubala, K. H., Christianson, J. P., Kaufman, R. D., Watkins, L. R., & Maier, S. F. (2012). Short- and long-term consequences of stressor controllability in adolescent rats. Behavioral Brain Research, 234(2), 278–284. https://doi.org/10.1016/j.bbr.2012.06.027Google Scholar
Kuramoto, E., Pan, S., Furuta, T., Tanaka, Y. R., Iwai, H., Yamanaka, A., Ohno, S., Kaneko, T., Goto, T., & Hioki, H. (2017). Individual mediodorsal thalamic neurons project to multiple areas of the rat prefrontal cortex: A single neuron-tracing study using virus vectors. Journal of Comparative Neurology, 525(1), 166–185. https://doi.org/10.1002/cne.24054Google Scholar
Lehmann, M. L., & Herkenham, M. (2011). Environmental enrichment confers stress resiliency to social defeat through an infralimbic cortex-dependent neuroanatomical pathway. Journal of Neuroscience, 31(16), 6159–6173. https://doi.org/10.1523/JNEUROSCI.0577-11.2011Google Scholar
Liljeholm, M., Tricomi, E., O’Doherty, J. P., & Balleine, B. W. (2011). Neural correlates of instrumental contingency learning: Differential effects of action-reward conjunction and disjunction. Journal of Neuroscience, 31(7), 2474–2480. https://doi.org/10.1523/JNEUROSCI.3354-10.2011Google Scholar
Lowry, C. A. (2002). Functional subsets of serotonergic neurones: Implications for control of the hypothalamic-pituitary-adrenal axis. Journal of Neuroendocrinology, 14(11), 911–923. https://doi.org/10.1046/j.1365-2826.2002.00861.xGoogle Scholar
Ly, V., Wang, K. S., Bhanji, J., & Delgado, M. R. (2019). A reward-based framework of perceived control. Frontiers in Neuroscience, 13, Article 65. https://doi.org/10.3389/fnins.2019.00065Google Scholar
Lyons, D. M., Parker, K. J., & Schatzberg, A. F. (2010). Animal models of early life stress: Implications for understanding resilience. Developmental Psychobiology, 52(7), 616–624. https://doi.org/10.1002/dev.20500Google Scholar
Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & Watkins, L. R. (1995). The dorsal raphe nucleus is a site of action mediating the behavioral effects of the benzodiazepine receptor inverse agonist DMCM. Behavioral Neuroscience, 109(4), 759–766. https://doi.org/10.1037//0735-7044.109.4.759Google Scholar
Maier, S. F., Grahn, R. E., & Watkins, L. R. (1995). 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock. Behavioral Neuroscience, 109(3), 404–412. https://doi.org/10.1037//0735-7044.109.3.404Google Scholar
Maier, S. F., Kalman, B. A., & Grahn, R. E. (1994). Chlordiazepoxide microinjected into the region of the dorsal raphe nucleus eliminates the interference with escape responding produced by inescapable shock whether administered before inescapable shock or escape testing. Behavioral Neuroscience, 108(1), 121–130. https://doi.org/10.1037//0735-7044.108.1.121Google Scholar
Maier, S. F., Ryan, S. M., Barksdale, C. M., & Kalin, N. H. (1986). Stressor controllability and the pituitary-adrenal system. Behavioral Neuroscience, 100(5), 669–674. https://doi.org/10.1037//0735-7044.100.5.669Google Scholar
Maier, S. F., & Seligman, M. E. P. (1976). Learned helplessness: Theory and evidence. Journal of Experimental Psychology: General, 105(1), 3–46. https://doi.org/10.1037/0096-3445.105.1.3Google Scholar
Maier, S. F., & Seligman, M. E. (2016). Learned helplessness at fifty: Insights from neuroscience. Psychological Review, 123(4), 349–367. https://doi.org/10.1037/rev0000033Google Scholar
Maier, S. F., Seligman, M. E. P., & Solomon, R. L. (1969). Pavlovian fear conditioning and learned helplessness: Effects on escape and avoidance behavior of (a) the CS-US contingency, and (b) the independence of the US and voluntary responding. In Campbell, B. A. & Church, R. M. (Eds.), Punishment and aversive behavior (pp. 299–342). Appleton-Century-Crofts.Google Scholar
Maier, S. F., & Watkins, L. R. (1998). Stressor controllability, anxiety, and serotonin. Cognitive Therapy and Research, 22(6), 595–613. https://doi.org/10.1023/A:1018794104325Google Scholar
Maswood, S., Barter, J. E., Watkins, L. R., & Maier, S. F. (1998). Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Research, 783(1), 115–120. https://doi.org/10.1016/s0006-8993(97)01313-9Google Scholar
McDevitt, R. A., Szot, P., Baratta, M. V., Bland, S. T., White, S. S., Maier, S. F., & Neumaier, J. F. (2009). Stress-induced activity in the locus coeruleus is not sensitive to stressor controllability. Brain Research, 1285, 109–118. https://doi.org/10.1016/j.brainres.2009.06.017Google Scholar
McRae, K., & Gross, J. J. (2020). Emotion regulation. Emotion, 20(1), 1–9. https://doi.org/10.1037/emo0000703Google Scholar
Milad, M. R., & Quirk, G. J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420, 70–74. https://doi.org/10.1038/nature01138Google Scholar
Minor, T. R., Dess, N. K., & Overmier, J. (1991). Inverting the traditional view of “learned helplessness. In Denny, M. R (Ed.), Fear, avoidance, and phobias: A fundamental analysis (pp. 87–133). Lawrence-Erlbaum Associates, Inc.Google Scholar
Nestler, E. J., & Waxman, S. G. (2020). Resilience to stress and resilience to pain: Lessons from molecular neurobiology and genetics. Trends in Molecular Medicine, 26(10), 924–935. https://doi.org/10.1016/j.molmed.2020.03.007Google Scholar
Quirk, G. J., Paré, D., Richardson, R., Herry, C., Monfils, M. H., Schiller, D., & Vicentic, A. (2010). Erasing fear memories with extinction training. Journal of Neuroscience, 30(45), 14993–14997. https://doi.org/10.1523/JNEUROSCI.4268-10.2010CrossRefGoogle ScholarPubMed
Ray, R. D., & Zald, D. H. (2012). Anatomical insights into the interaction of emotion and cognition in the prefrontal cortex. Neuroscience & Biobehavioral Reviews, 36(1), 479–501. https://doi.org/10.1016/j.neubiorev.2011.08.005Google Scholar
Ressler, R. L., & Maren, S. (2019). Synaptic encoding of fear memories in the amygdala. Current Opinion in Neurobiology, 54, 54–59. https://doi.org/10.1016/j.conb.2018.08.012CrossRefGoogle ScholarPubMed
Rogan, M. T., Leon, K. S., Perez, D. L., & Kandel, E. R. (2005). Distinct neural signatures for safety and danger in the amygdala and striatum of the mouse. Neuron, 46(2), 309–320. https://doi.org/10.1016/j.neuron.2005.02.017Google Scholar
Rozeske, R. R., Evans, A. K., Frank, M. G., Watkins, L. R., Lowry, C. A., & Maier, S. F. (2011). Uncontrollable, but not controllable, stress desensitizes 5-HT1A receptors in the dorsal raphe nucleus. Journal of Neuroscience, 31(2), 14107–14115. https://doi.org/10.1523/JNEUROSCI.3095-11.2011Google Scholar
Sawchenko, P. E., Swanson, L. W., Steinbusch, H. W., & Verhofstad, A. A. (1983). The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat. Brain Research, 277(2), 355–360. https://doi.org/10.1016/0006-8993(83)90945-9Google Scholar
Schoenberg, H. L., Sola, E. X., Seyller, E., Kelberman, M., & Toufexis, D. J. (2019). Female rats express habitual behavior earlier in operant training than males. Behavioral Neuroscience, 133(1), 110–120. https://doi.org/10.1037/bne0000282Google Scholar
Seligman, M. E., & Maier, S. F. (1967). Failure to escape traumatic shock. Journal of Experimental Psychology, 74(1), 1–9. https://doi.org/10.1037/h0024514Google Scholar
Strong, P. V., Christianson, J. P., Loughridge, A. B., Amat, J., Maier, S. F., Fleshner, M., & Greenwood, B. N. (2011). 5-hydroxytryptamine 2C receptors in the dorsal striatum mediate stress-induced interference with negatively reinforced instrumental escape behavior. Neuroscience, 197, 132–144. https://doi.org/j.neuroscience.2011.09.041Google Scholar
Tanner, M. K., Fallon, I. P., Baratta, M. V., & Greenwood, B. N. (2019). Voluntary exercise enables stress resistance in females. Behavioral Brain Research, 369, Article 111923. https://doi.org/10.1016/j.bbr.2019.111923Google Scholar
Targum, S. D., & Nemeroff, C. B. (2019). The effect of early life stress on adult psychiatric disorders. Innovations in Clinical Neuroscience, 16(1–2), 35–37.Google Scholar
Thompson, R. S., Christianson, J. P., Maslanik, T. M., Maier, S. F., Greenwood, B. N., & Fleshner, M. (2013). Effects of stressor controllability on diurnal physiological rhythms. Physiology & Behavior, 112–113, 32–39. https://doi.org/10.1016/j.physbeh.2013.02.009Google Scholar
Troy, A. S., Wilhelm, F. H., Shallcross, A. J., & Mauss, I. B. (2010). Seeing the silver lining: Cognitive reappraisal ability moderates the relationship between stress and depressive symptoms. Emotion, 10(6), 783–795. https://doi.org/10.1037/a0020262Google Scholar
Uribe-Mariño, A., Gassen, N. C., Wiesbeck, M. F., Balsevich, G., Santarelli, S., Solfrank, B., Dournes, C., Fries, G. R., Masana, M., Labermeier, C., Wang, X. D., Hafner, K., Schmid, B., Rein, T., Chen, A., Deussing, J. M., & Schmidt, M. V. (2016). Prefrontal cortex corticotropin-releasing factor receptor 1 conveys acute stress-induced executive dysfunction. Biological Psychiatry, 80(10), 743–753. https://doi.org/10.1016/j.biopsych.2016.03.2106Google Scholar
Urry, H. L., van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., Jackson, C. A., Frye, C. J., Greischar, L. L., Alexander, A. L., & Davidson, R. J. (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience, 26(16), 4415–4425. https://doi.org/10.1523/JNEUROSCI.3215-05.2006Google Scholar
Valentino, R. J., Bangasser, D., & Van Bockstaele, E. J. (2013). Sex-biased stress signaling: The corticotropin-releasing factor receptor as a model. Molecular Pharmacology, 83(4), 737–745. https://doi.org/10.1124/mol.112.083550Google Scholar
Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51(11), 32–58. https://doi.org/10.1002/syn.10279Google Scholar
Vialou, V., Bagot, R. C., Cahill, M. E., Ferguson, D., Robison, A. J., Dietz, D. M., Fallon, B., Mazei-Robison, M., Ku, S. M., Harrigan, E., Winstanley, C. A., Joshi, T., Feng, J., Berton, O., & Nestler, E. J. (2014). Prefrontal cortical circuit for depression- and anxiety-related behaviors mediated by cholecystokinin: Role of ΔFosB. Journal of Neuroscience, 34(11), 3878–3887. https://doi.org/10.1523/JNEUROSCI.1787-13.2014Google Scholar
Wang, K. S., & Delgado, M. R. (2019). Corticostriatal circuits encode the subjective value of perceived control. Cerebral Cortex, 29(12), 5049–5060. https://doi.org/10.1093/cercor/bhz045Google Scholar
Weiss, J. M. (1968). Effects of coping responses on stress. Journal of Comparative and Physiological Psychology, 65(1), 251–260. https://doi.org/10.1037/h0025562Google Scholar
Weiss, J. M. (1971). Effects of coping behavior with and without a feedback signal on stress pathology in rats. Journal of Comparative and Physiological Psychology, 77(1), 22–30. https://doi.org/10.1037/h0031581Google Scholar
White, J., Pearce, J., Morrison, S., Dunstan, F., Bisson, J. I., & Fone, D. L. (2015). Risk of post-traumatic stress disorder following traumatic events in a community sample. Epidemiology and Psychiatric Sciences, 24(3), 249–257. https://doi.org/10.1017/S2045796014000110Google Scholar
Williams, J. L., & Maier, S. F. (1977). Transituational immunization and therapy of learned helplessness in the rat. Journal of Experimental Psychology: Animal Behavior Processes, 3(3), 240–252. https://doi.org/10.1037/0097-7403.3.3.240Google Scholar
Woodmansee, W. W., Silbert, L. H., & Maier, S. F. (1993). Factors that modulate inescapable shock-induced reductions in daily activity in the rat. Pharmacology Biochemistry and Behavior, 45(3), 553–559. https://doi.org/10.1016/0091-3057(93)90505-nGoogle Scholar
Zeeni, N., Bassil, M., Fromentin, G., Chaumontet, C., Darcel, N., Tome, D., Daher, C. F. (2015). Environmental enrichment and cafeteria diet attenuate the response to chronic variable stress in rats. Physiology & Behavior, 139, 41–49. https://doi.org/10.1016/j.physbeh.2014.11.003Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×