Advertisement

Cognitive, Affective, & Behavioral Neuroscience

, Volume 13, Issue 3, pp 501–518 | Cite as

Amygdala functional connectivity is reduced after the cold pressor task

  • David ClewettEmail author
  • Andrej Schoeke
  • Mara Mather
Article

Abstract

The amygdala forms a crucial link between central pain and stress systems. Previous research indicates that psychological stress affects amygdala activity, but it is less clear how painful stressors influence subsequent amygdala functional connectivity. In the present study, we used pulsed arterial spin labeling (PASL) to investigate differences in healthy male adults’ resting-state amygdala functional connectivity following a cold pressor versus a control task, with the stressor and control conditions being conducted on different days. During the period of peak cortisol response to acute stress (approximately 15–30 min after stressor onset), participants were asked to rest for 6 min with their eyes closed during a PASL scanning sequence. The cold pressor task led to reduced resting-state functional connectivity between the amygdalae and orbitofrontal cortex (OFC) and ventromedial prefrontal cortex, and this occurred irrespective of cortisol release. The stressor also induced greater inverse connectivity between the left amygdala and dorsal anterior cingulate cortex (ACC), a brain region implicated in the down-regulation of amygdala responsivity. Furthermore, the degree of poststressor left amygdala decoupling with the lateral OFC varied according to self-reported pain intensity during the cold pressor task. These findings indicate that the cold pressor task alters amygdala interactions with prefrontal and ACC regions 15–30 min after the stressor, and that these altered functional connectivity patterns are related to pain perception rather than cortisol feedback.

Keywords

Amygdala Stress Pain Functional connectivity Arterial spin labeling Cold pressor task 

Notes

Author note

We thank Zara Abrams for her assistance with scanning, and Jonathan Dayka and Rico Velasco for their assistance with creating the figures. This research was supported by NIA Grant Nos. R01AG038043 and K02AG032309.

Supplementary material

13415_2013_162_MOESM1_ESM.doc (649 kb)
ESM 1 (DOC 649 kb)

References

  1. Aguirre, G. K., Detre, J. A., Zarahn, E., & Alsop, D. C. (2002). Experimental design and the relative sensitivity of BOLD and perfusion fMRI. NeuroImage, 15, 488–500.PubMedCrossRefGoogle Scholar
  2. al’Absi, M., Hugdahl, K., & Lovallo, W. R. (2002). Adrenocortical stress responses and altered working memory performance. Psychophysiology, 39, 95–99.PubMedCrossRefGoogle Scholar
  3. al’Absi, M., Wittmers, L. E., Ellestad, D., Nordehen, G., Do, S. W. K., Kirschbaum, C., & Grant, J. E. (2004). Sex differences in pain and hypothalamic–pituitary–adrenocortical responses to opioid blockade. Psychosomatic Medicine, 66, 198–206.PubMedCrossRefGoogle Scholar
  4. Aloisi, A. M., & Bonifazi, M. (2006). Sex hormones, central nervous system and pain. Hormones and Behavior, 50, 1–7. doi: 10.1016/j.yhbeh.2005.12.002 PubMedCrossRefGoogle Scholar
  5. Amaral, D. G., & Price, J. L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). The Journal of Comparative Neurology, 230, 465–496.PubMedCrossRefGoogle Scholar
  6. Anderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305–309. doi: 10.1038/35077083 PubMedCrossRefGoogle Scholar
  7. Beckmann, C. F., DeLuca, M., Devlin, J. T., & Smith, S. M. (2005). Investigations into resting- state connectivity using independent component analysis. Philosophical Transactions of the Royal Society B, 360, 1001–1013.CrossRefGoogle Scholar
  8. Bernard, J. F., & Besson, J. M. (1988). Convergence of nociceptive information on the parabrachio-amygdala neurons in the rat. Comptes Rendus de l’Académie des Sciences: Serie III, 307, 841–847.Google Scholar
  9. Bernard, J. F., Huang, G. F., & Besson, J. M. (1992). Nucleus centralis of the amygdala and the globus pallidus ventralis: Electrophysiological evidence for an involvement in pain processes. Journal of Neurophysiology, 68, 551–569.PubMedGoogle Scholar
  10. Bingel, U., & Tracey, I. (2008). Imaging CNS modulation of pain in humans. Physiology, 23, 371–380. doi: 10.1152/physiol.00024.2008 PubMedCrossRefGoogle Scholar
  11. Blalock, H. (1972). Social statistics. New York, NY: McGraw-Hill.Google Scholar
  12. Blandini, F., Martignoni, E., Sances, E., Bono, G., & Nappi, G. (1995). Combined response of plasma and platelet catecholamines to different types of short-term stress. Life Sciences, 56, 1113–1120.PubMedCrossRefGoogle Scholar
  13. Bornhovd, K., Quante, M., Glauche, V., Bromm, B., Weiller, C., & Buchel, C. (2002). Painful stimuli evoke different stimulus–response functions in the amygdala, prefrontal, insula and somatosensory cortex: A single-trial fMRI study. Brain, 125, 1326–1336.PubMedCrossRefGoogle Scholar
  14. Boyle, M. P., Brewer, J. A., Fanatsu, M., Wozniak, D. F., Tsien, J. Z., Izumi, Y., & Muglia, L. J. (2005). Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proceedings of the National Academy of Sciences, 102, 473–478.CrossRefGoogle Scholar
  15. Buchanan, T. W., Tranel, D., & Adolphs, R. (2006). Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning and Memory, 13, 382–387.PubMedCrossRefGoogle Scholar
  16. Burgmer, M., Gaubitz, M., Konrad, C., Wrenger, M., Hilgart, S., Heuft, G., & Pfleiderer, B. (2009). Decreased gray matter volumes in the cingulo-frontal cortex and the amygdala in patients with fibromyalgia. Psychosomatic Medicine, 71, 566–573. doi: 10.1097/PSY.0b013e3181a32da0 PubMedCrossRefGoogle Scholar
  17. Cavada, C., Tejedor, J., Cruz-Rizzolo, R. J., & Reinoso-Suárez, F. (2000). The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cerebral Cortex, 10, 220–242.PubMedCrossRefGoogle Scholar
  18. Coghill, R. C., McHaffie, J. G., & Yen, Y. F. (2003). Neural correlates of interindividual differences in the subjective experience of pain. Proceedings of the National Academy of Sciences, 100, 8538–8542.CrossRefGoogle Scholar
  19. Davis, M., Walker, D. L., Miles, L., & Grillon, C. (2010). Phasic vs. sustained fear in rats and humans: Role of the extended amygdala in fear vs. anxiety. Neuropsychopharmacology, 35, 105–135.PubMedCrossRefGoogle Scholar
  20. de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999). Stress and cognition: Are corticosteroids good or bad guys? Trends in Neurosciences, 22, 422–426.PubMedCrossRefGoogle Scholar
  21. de Kloet, E. R., & Reul, J. M. (1987). Feedback action and tonic influence of corticosteroids on brain function: A concept arising from the heterogeneity of brain receptor systems. Psychoneuroendocrinology, 12, 83–105.PubMedCrossRefGoogle Scholar
  22. Derbyshire, S. W., Jones, A. K., Gyulai, F., Clark, S., Townsend, D., & Firestone, L. L. (1997). Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain, 73, 431–445.PubMedCrossRefGoogle Scholar
  23. Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391.PubMedCrossRefGoogle Scholar
  24. Diorio, D., Viau, V., & Meaney, M. J. (1993). The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. Journal of Neuroscience, 13, 3839–3847.PubMedGoogle Scholar
  25. Dixon, K. E., Thorn, B. E., & Ward, L. C. (2004). An evaluation of sex differences in psychological and physiological responses to experimentally-induced pain: A path analytic description. Pain, 112, 188–196. doi: 10.1016/j.pain.2004.08.017 PubMedCrossRefGoogle Scholar
  26. Donahue, M. J., Lu, H., Jones, C. K., Pekar, J. J., & van Zijl, P. C. (2006). An account of the discrepancy between MRI and PET cerebral blood flow measures. A high-field MRI investigation. NMR in Biomedicine, 19, 1043–1054.PubMedCrossRefGoogle Scholar
  27. Drolet, G., Dumon, E. C., Gosselin, I., Kinhead, R., Laforest, S., & Trottier, J. F. (2001). Role of endogenous opioid system in the regulation of the stress response. Science, 25, 729–741.Google Scholar
  28. Duncko, R., Cornwell, B., Cui, L., Merikangas, K. R., & Grillon, C. (2007). Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learning and Memory, 14, 329–335.PubMedCrossRefGoogle Scholar
  29. Duncko, R., Johnson, L., Merikangas, K., & Grillon, C. (2009). Working memory performance after acute exposure to the cold pressor stress in healthy volunteers. Neurobiology of Learning and Memory, 91, 377–381.PubMedCrossRefGoogle Scholar
  30. Eryilmaz, H., Van de Ville, D., Schwartz, S., & Vuilleumier, P. (2011). Impact of transient emotions on functional connectivity during subsequent resting state: A wavelet correlation approach. NeuroImage, 54, 2481–2491. doi: 10.1016/j.neuroimage.2010.10.021 PubMedCrossRefGoogle Scholar
  31. Etkin, A., Egner, T., & Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15, 85–93. doi: 10.1016/j.tics.2010.11.004 PubMedCrossRefGoogle Scholar
  32. Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51, 871–882.PubMedCrossRefGoogle Scholar
  33. Fields, H. L. (2004). State-dependent opioid control of pain. Nature Reviews Neuroscience, 5, 565–575.PubMedCrossRefGoogle Scholar
  34. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences, 102, 9673–9678.CrossRefGoogle Scholar
  35. Frew, A. K., & Drummond, P. D. (2007). Negative affect, pain and sex: The role of endogenous opioids. Pain, 132, 77–85.CrossRefGoogle Scholar
  36. Ghashghaei, H. T., & Barbas, H. (2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115, 1261–1279.PubMedCrossRefGoogle Scholar
  37. Hapidou, E. G., & De Catanzaro, D. (1988). Sensitivity to cold pressor pain in dysmenorrheic and non-dysmenorrheic women as a function of menstrual cycle phase. Pain, 34, 277–283.PubMedCrossRefGoogle Scholar
  38. Hardy, J. D., Wolff, H. G., & Goodell, H. (1952). Pain sensations and reactions. Baltimore, MD: Williams & Wilkins.Google Scholar
  39. Hariri, A. R., Mattay, V. S., Tessitore, A., Fera, F., & Weinberger, D. R. (2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry, 53, 494–501.PubMedCrossRefGoogle Scholar
  40. Hellström, B., & Lundberg, U. (2000). Pain perception to the cold pressor test during the menstrual cycle in relation to estrogen levels and a comparison with men. Integrative Physiological and Behavioral Science, 35, 132–141.PubMedCrossRefGoogle Scholar
  41. Henckens, M. J., van Wingen, G. A., Joëls, M., & Fernández, G. (2012). Corticosteroid induced decoupling of the amygdala in men. Cerebral Cortex, 22, 2336–2345. doi: 10.1093/cercor/bhr313 PubMedCrossRefGoogle Scholar
  42. Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo–pituitary–adrenocortical axis. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 29, 1201–1213.CrossRefGoogle Scholar
  43. Hutchinson, W. D., Davis, K. D., Lozano, A. M., Tasker, R. R., & Dostrovsky, J. O. (1999). Pain-related neurons in the human cingulated cortex. Nature Neuroscience, 2, 403–405.CrossRefGoogle Scholar
  44. Ikeda, R., Takahashi, Y., Inoue, K., & Kato, F. (2007). NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain, 127, 161–172. doi: 10.1016/j.pain.2006.09.003 PubMedCrossRefGoogle Scholar
  45. Johnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., & Davidson, R. J. (2007). Failure to regulate: Counterproductive recruitment of top-down prefrontal–subcortical circuitry in major depression. Journal of Neuroscience, 27, 8877–8884.PubMedCrossRefGoogle Scholar
  46. Kern, S., Oakes, T. R., Stone, C. K., McAuliff, E. M., Kirschbaum, C., & Davidson, R. J. (2008). Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor. Psychoneuroendocrinology, 33, 517–529.PubMedCrossRefGoogle Scholar
  47. Kilpatrick, L. A., Zald, D. H., Pardo, J. V., & Cahill, L. F. (2006). Sex-related differences in amygdala functional connectivity during resting conditions. NeuroImage, 30, 452–461. doi: 10.1016/j.neuroimage.2005.09.065 PubMedCrossRefGoogle Scholar
  48. Kringelbach, M. L., & Rolls, E. T. (2004). The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology. Progress in Neurobiology, 72, 341–372.PubMedCrossRefGoogle Scholar
  49. Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: A review. Biological Psychology, 69, 113–132.PubMedCrossRefGoogle Scholar
  50. Lapate, R. C., Lee, H., Salomons, T. V., van Reekum, C. M., Greischar, L. L., & Davidson, R. J. (2012). Amygdalar function reflects common individual differences in emotion and pain regulation success. Journal of Cognitive Neuroscience, 24, 148–158.PubMedCrossRefGoogle Scholar
  51. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. doi: 10.1146/annurev.neuro.23.1.155 PubMedCrossRefGoogle Scholar
  52. LeDoux, J. (2003). The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology, 23, 727–738.PubMedCrossRefGoogle Scholar
  53. Lee, H., Heller, A. S., van Reekum, C. M., Nelson, B., & Davidson, R. J. (2012). Amygdala–prefrontal coupling underlies individual differences in emotion regulation. NeuroImage, 62, 1575–1581.PubMedCrossRefGoogle Scholar
  54. Leknes, S., Brooks, J. C., Wiech, K., & Tracey, I. (2008). Pain relief as an opponent process: A psychophysical investigation. European Journal of Neuroscience, 28, 794–801.PubMedCrossRefGoogle Scholar
  55. Lenz, F. A., Rios, M., Zirh, A., Chau, D., Krauss, G., & Lesser, R. P. (1998). Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus. Journal of Neurophysiology, 79, 2231–2234.PubMedGoogle Scholar
  56. Liddell, B. J., Brown, K. J., Kemp, A. H., Barton, M. J., Das, P., Peduto, A., … Williams, L. M. (2005). A direct brainstem–amygdala–cortical “alarm” system for subliminal signals of fear. NeuroImage, 24, 235–243.Google Scholar
  57. Lighthall, N. R., Gorlick, M. A., Schoeke, A., Frank, M. J., & Mather, M. (2013). Stress modulates reinforcement learning in younger and older adults. Psychology and Aging, 28(1), 35–46Google Scholar
  58. Lighthall, N. R., Mather, M., & Gorlick, M. A. (2009). Acute stress increases sex differences in risk seeking in the Balloon Analogue Risk Task. PLoS One, 4, e6002. doi: 10.1371/journal.pone.0006002 PubMedCrossRefGoogle Scholar
  59. Lighthall, N. R., Sakaki, M., Vasunilashorn, S., Nga, L., Somayajula, S., Chen, … Mather, M. (2011). Gender differences in reward-related decision processing under stress. Social Cognitive and Affective Neuroscience, 7, 476–484.Google Scholar
  60. Lovallo, W. R., Robinson, J. L., Glahn, D. C., & Fox, P. T. (2010). Acute effects of hydrocortisone on the human brain: An fMRI study. Psychoneuroendocrinology, 35, 15–20.PubMedCrossRefGoogle Scholar
  61. Luh, W. M., Wong, E. C., Bandettini, P. A., & Hyde, J. S. (1999). QUIPSS II with thin-slice TI1 periodic saturation: A method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magnetic Resonance in Medicine, 41, 1246–1254.PubMedCrossRefGoogle Scholar
  62. Maihofner, C., & Handwerker, H. O. (2005). Differential coding of hyperalgesia in the human brain: A functional MRI study. NeuroImage, 28, 996–1006.PubMedCrossRefGoogle Scholar
  63. Mather, M., Gorlick, M. A., & Lighthall, N. R. (2009). To brake or accelerate when the light turns yellow? Stress reduces older adults’ risk taking in a driving game. Psychological Science, 20, 174–176. doi: 10.1111/j.1467-9280.2009.02275.x PubMedCrossRefGoogle Scholar
  64. Mather, M., Lighthall, N. R., Nga, L., & Gorlick, M. A. (2010). Sex differences in how stress affects brain activity during face viewing. NeuroReport, 21, 933–937. doi: 10.1097/WNR.0b013e32833ddd92 PubMedCrossRefGoogle Scholar
  65. May, A. (2011). Structural brain imaging: A window into chronic pain. The Neuroscientist, 17, 209–220.PubMedCrossRefGoogle Scholar
  66. McDonald, A. J., Mascagni, F., & Guo, L. (1996). Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience, 71, 55–75. doi: 10.1016/0306-4522(95)00417-3 PubMedCrossRefGoogle Scholar
  67. McRae, A. L., Saladin, M. E., Brady, K. T., Upadhyaya, H., Back, S. E., & Timmermann, M. A. (2006). Stress reactivity: Biological and subjective responses to the cold pressor and trier social stressors. Human Psychopharmacology, 21, 377–385.PubMedCrossRefGoogle Scholar
  68. Mitsushima, D., Yamada, K., Takase, K., Funabashi, T., & Kimura, F. (2006). Sex differences in the basolateral amygdala: The extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. European Journal of Neuroscience, 24, 3245–3254.PubMedCrossRefGoogle Scholar
  69. Modinos, G., Ormel, J., & Aleman, A. (2010). Individual differences in dispositional mindfulness and brain activity involved in reappraisal of emotion. Social Cognitive and Affective Neuroscience, 5, 369–377.PubMedCrossRefGoogle Scholar
  70. Mumford, J. A., Hernandez-Garcia, L., Lee, G. R., & Nichols, T. E. (2006). Estimation efficiency and statistical power in arterial spin labeling fMRI. NeuroImage, 33, 103–114.PubMedCrossRefGoogle Scholar
  71. Neugebauer, V., & Li, W. (2003). Differential sensitization of amygdala neurons to afferent inputs in a model of arthritic pain. Journal of Neurophysiology, 89, 716–727.PubMedCrossRefGoogle Scholar
  72. Neugebauer, V., Li, W., Bird, G. C., & Han, J. S. (2004). The amygdala and persistent pain. The Neuroscientist, 10, 221–234.PubMedCrossRefGoogle Scholar
  73. Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Rethinking feelings: An fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215–1229. doi: 10.1162/089892902760807212 PubMedCrossRefGoogle Scholar
  74. Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D. E., & Gross, J. J. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23, 483–499. doi: 10.1016/j.neuroimage.2004.06.030 PubMedCrossRefGoogle Scholar
  75. Pascualy, M., Petrie, E. C., Brodkin, K., Peskind, E. R., Wilkinson, C. W., & Raskind, M. A. (2000). Hypothalamic pituitary adrenocortical and sympathetic nervous system responses to the cold pressor test in Alzheimer’s disease. Biological Psychiatry, 48, 247–254.PubMedCrossRefGoogle Scholar
  76. Petrovic, P., Carlsson, K., Petersson, K. M., Hansson, P., & Ingvar, M. (2004). Context-dependent deactivation of the amygdala during pain. Journal of Cognitive Neuroscience, 16, 1289–1301.PubMedCrossRefGoogle Scholar
  77. Petrovic, P., & Ingvar, M. (2002). Imaging cognitive modulation of pain processing. Pain, 95, 1–5.PubMedCrossRefGoogle Scholar
  78. Porcelli, A. J., Cruz, D., Wenberg, K., Patterson, M. D., Biswal, B. B., & Rypma, B. (2008). The effects of acute stress on human prefrontal working memory systems. Physiology and Behavior, 95, 282–289.PubMedCrossRefGoogle Scholar
  79. Price, D. D., & Barrell, J. J. (2000). Mechanisms of analgesia produced by hypnosis and placebo suggestions. Progress in Brain Research, 122, 255–271.PubMedCrossRefGoogle Scholar
  80. Rainville, P., Duncan, G. H., Price, D. D., Carrier, B., & Bushnell, M. C. (1997). Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science, 277, 968–971.PubMedCrossRefGoogle Scholar
  81. Robinson, J. L., Laird, A. R., Glahn, D. C., Lovallo, W. R., & Fox, P. T. (2010). Meta-analytic connectivity modeling: Delineating the functional connectivity of the human amygdala. Human Brain Mapping, 31, 173–184. doi: 10.1002/hbm.20854 PubMedGoogle Scholar
  82. Roger, D., & Najarian, B. (1998). The relationship between emotional rumination and cortisol secretion under stress. Personality and Individual Differences, 24, 531–538.CrossRefGoogle Scholar
  83. Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, M. C., Uddin, L. Q., Gotimer, K., … Milham, M. P. (2009). Functional connectivity of the human amygdala using resting state fMRI. NeuroImage, 45, 614–626.Google Scholar
  84. Rule, R. R., Shimamura, A. P., & Knight, R. T. (2002). Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cognitive, Affective, & Behavioral Neuroscience, 2, 264–270. doi: 10.3758/CABN.2.3.264 CrossRefGoogle Scholar
  85. Salomons, T. V., Johnstone, T., Backonja, M. M., Shackman, A. J., & Davidson, R. J. (2007). Individual differences in the effects of perceived controllability on pain perception: Critical role of the prefrontal cortex. Journal of Cognitive Neuroscience, 19, 993–1003.PubMedCrossRefGoogle Scholar
  86. Sapolsky, R. M. (1996). Why stress is bad for your brain. Science, 273, 749–750.PubMedCrossRefGoogle Scholar
  87. Schwabe, L., Haddad, L., & Schachinger, H. (2008). HPA axis activation by a socially evaluated cold pressor test. Psychoneuroendocrinology, 33, 890–895.PubMedCrossRefGoogle Scholar
  88. Stein, J. L., Wiedholz, L. M., Bassett, D. S., Weinberger, D. R., Zink, C. F., Mattay, V. S., & Meyer-Lindenberg, A. (2007). A validated network of effective amygdala connectivity. NeuroImage, 36, 736–745.PubMedCrossRefGoogle Scholar
  89. Talbot, J. D., Villemure, J. G., Bushnell, M. C., & Duncan, G. H. (1995). Evaluation of pain perception after anterior capsulotomy: A case report. Somatosensory and Motor Research, 12, 115–126.PubMedCrossRefGoogle Scholar
  90. Tavernor, S. J., Abduljawad, K. A. J., Langley, R. W., Bradshaw, C. M., & Szabadi, E. (2000). Effects of pentagastrin and the cold pressor test on the acoustic startle response and pupillary function in man. Journal of Psychopharmacology, 14, 387–394.PubMedCrossRefGoogle Scholar
  91. Thorpe, S. J., Rolls, E. T., & Maddison, S. (1983). The orbitofrontal cortex: Neuronal activity in the behaving monkey. Experimental Brain Research, 49, 93–115.CrossRefGoogle Scholar
  92. Urry, H. L., van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., … 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, 4415–4425. doi: 10.1523/JNEUROSCI.3215-05.2006
  93. van Marle, H. J., Hermans, E. J., Qin, S., & Fernández, G. (2010). Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. NeuroImage, 53, 348–354. doi: 10.1016/j.neuroimage.2010.05.070 PubMedCrossRefGoogle Scholar
  94. Veer, I. M., Oei, N. Y. L., Spinhoven, P., van Buchem, M. A., Elzinga, B. M., & Rombouts, S. A. R. B. (2011a). Beyond acute social stress: Increased functional connectivity between amygdala and cortical midline structures. NeuroImage, 57, 1534–1541. doi: 10.1016/j.neuroimage.2011.05.074 PubMedCrossRefGoogle Scholar
  95. Veer, I. M., Oei, N. Y. L., Spinhoven, P., van Buchem, M. A., Elzinga, B. M., & Rombouts, S. A. R. B. (2011b). Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex. Psychoneuroendocrinology, 37, 1039–1047. doi: 10.1016/j.psyneuen.2011.12.001 PubMedCrossRefGoogle Scholar
  96. Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51, 32–58.PubMedCrossRefGoogle Scholar
  97. Vogt, B. A., & Pandya, D. N. (1987). Cingulate cortex of the rhesus monkey: II. Cortical afferents. Journal of Comparative Neurology, 262, 271–289.PubMedCrossRefGoogle Scholar
  98. Wang, J., Aguirre, G. K., Kimberg, D. Y., Roc, A. C., Li, L., & Detre, J. A. (2003). Arterial spin labeling perfusion fMRI with very low task frequency. Magnetic Resonance in Medicine, 49, 796–802.PubMedCrossRefGoogle Scholar
  99. Wang, Z., Guo, Y., Bradesi, S., Labus, J. S., Maarek, J. M. I., Lee, K.,… Holschneider, D. (2009). Sex differences in functional brain activation during noxious visceral stimulation in rats. Pain, 145, 120–128.Google Scholar
  100. Wang, J., Li, L., Roc, A. C., Alsop, D. C., Tang, K., Butler, N. S., … Detre, J. A. (2004). Reduced susceptibility effects in perfusion fMRI with single-shot spin-echo EPI acquisitions at 1.5 tesla. Magnetic Resonance Imaging, 22, 1–7.Google Scholar
  101. Watkins, L. R., & Mayer, D. J. (1982). Organization of endogenous opiate and nonopiate pain control systems. Science, 216, 1185–1192.PubMedCrossRefGoogle Scholar
  102. Watson, D., Clark, L. A., & Tellegan, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychology, 54, 1063–1070. doi: 10.1037/0022-3514.54.6.1063 PubMedCrossRefGoogle Scholar
  103. Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience, 18, 411–418.PubMedGoogle Scholar
  104. Wiech, K., Kalisch, R., Weiskopf, N., Pleger, B., Stephan, K. E., & Dolan, R. J. (2006). Anterolateral prefrontal cortex mediates the analgesic effect of expected and perceived control over pain. Journal of Neuroscience, 26, 11501–11509.PubMedCrossRefGoogle Scholar
  105. Wong, E. C., Buxton, R. B., & Frank, L. R. (1997). Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR in Biomedicine, 10, 237–249.PubMedCrossRefGoogle Scholar
  106. Wong, E. C., Buxton, R. B., & Frank, L. R. (1998). Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magnetic Resonance in Medicine, 39, 702–708.PubMedCrossRefGoogle Scholar
  107. Xie, Y. F., Huo, F. Q., & Tang, J. S. (2009). Cerebral cortex modulation of pain. Acta Pharmacologica Sinica, 30, 31–41.PubMedCrossRefGoogle Scholar
  108. Zappe, A. C., Pfeuffer, J., Merkle, H., Logothetis, N. K., & Goense, J. B. M. (2008). The effect of labeling parameters on perfusion-based fMRI in nonhuman primates. Journal of Cerebral Blood Flow and Metabolism, 28, 640–652.PubMedCrossRefGoogle Scholar
  109. Zhang, Y., Tang, J., Yuan, B., & Jia, H. (1997). Inhibitory effects of electrically evoked activation of ventrolateral orbital cortex on the tail-flick reflex are mediated by periaqueductal gray in rats. Pain, 72, 127–135.PubMedCrossRefGoogle Scholar
  110. Zoccola, P. M., Dickerson, S. S., & Zaldivar, F. P. (2008). Rumination and cortisol responses to laboratory stressors. Psychosomatic Medicine, 70, 661–667.PubMedCrossRefGoogle Scholar
  111. Zubieta, J. K., Bueller, J. A., Jackson, L. R., Scott, D. J., Xu, Y., Koeppe, R. A., … Stohler, C. S. (2005). Placebo effects mediated by endogenous opioid activity on mu-opioid receptors. Journal of Neuroscience, 25, 7754–7762.Google Scholar
  112. Zubieta, J., Smith, Y. R., Bueller, J. A., Xu, Y., Kilbourn, M. R., Jewett, D., … Stohler, C. S. (2002). Mu-opioid receptor-mediated antinociceptive responses differ in men and women. Journal of Neuroscience, 22, 5100–5107.Google Scholar

Copyright information

© Psychonomic Society, Inc. 2013

Authors and Affiliations

  1. 1.University of Southern CaliforniaLos AngelesUSA
  2. 2.Free University of BerlinBerlinGermany
  3. 3.Neuroscience Graduate ProgramUniversity of Southern CaliforniaLos AngelesUSA

Personalised recommendations