Functional MRI Techniques Suggesting that the Stress System Interacts with Three Large Scale Core Brain Networks to Help Coordinate the Adaptive Response: A Systematic Review


Cite item

Full Text

Abstract

Objective:Synthesis of functional MRI (fMRI) and functional connectivity (FC) analysis data on human stress system (SS) function, as it relates to the dynamic function of the Salience (SN), Default Mode (DMN) and Central Executive (CEN) networks.

Methods:Systematic search of Medline, Scopus, Clinical Trials.gov, and Google Scholar databases of studies published prior to September 2022 resulted in 28 full-text articles included for qualitative synthesis.

Results:Acute stress changes the states of intra-/inter- neural network FCs and activities from those of resting, low arousal state in the SN, DMN and CEN, during which intra- and inter-network FCs and activities of all three networks are low. SS activation is positively linked to the activity of the SN and negatively to that of the DMN, while, in parallel, it is associated with an initial decrease and a subsequent increase of the intra- network FC and activity of the CEN. The FC between the DMN and the CEN increases, while those between the SN and the CEN decrease, allowing time for frontal lobe strategy input and "proper" CEN activity and task decision. SN activation is linked to sensory hypersensitivity, "impaired" memory, and a switch from serial to parallel processing, while trait mindfulness is associated with FC changes promoting CEN activity and producing a "task-ready state".

Conclusion:SS activation is tightly connected to that of the SN, with stress hormones likely potentiating the intra-network FC of the latter, attenuating that of the DMN, and causing a biphasic suppression- to-activation response of the CEN, all adaptive changes favoring proper decisions and survival.

About the authors

George Paltoglou

Medical School, Medical School, National and Kapodistrian University of Athens, "Aghia Sophia" Children's Hospital

Author for correspondence.
Email: info@benthamscience.net

Charikleia Stefanaki

Medical School, University Research Institute of Maternal and Child Health and Precision Medicine, National and Kapodistrian University of Athens

Email: info@benthamscience.net

George Chrousos

Medical School, University Research Institute of Maternal and Child Health and Precision Medicine, Medical School, National and Kapodistrian University of Athens

Email: info@benthamscience.net

References

  1. Chrousos, G.P.; Gold, P.W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA, 1992, 267(9), 1244-1252. doi: 10.1001/jama.1992.03480090092034 PMID: 1538563
  2. Cobb, M. A brief history of wires in the brain. Front. Ecol. Evol., 2021, 9, 760269. doi: 10.3389/fevo.2021.760269
  3. Ludwig, P.E.; Reddy, V.; Varacallo, M. Neuroanatomy, Central Nervous System (CNS). In: StatPearls; Treasure Island (FL): StatPearls Publishing, 2022.
  4. Sporns, O.; Tononi, G.; Kötter, R. The human connectome: A structural description of the human brain. PLOS Comput. Biol., 2005, 1(4), e42. doi: 10.1371/journal.pcbi.0010042 PMID: 16201007
  5. Kim, S.Y.; Chung, K.; Deisseroth, K. Light microscopy mapping of connections in the intact brain. Trends Cogn. Sci., 2013, 17(12), 596-599. doi: 10.1016/j.tics.2013.10.005 PMID: 24210964
  6. Chrousos, G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol., 2009, 5(7), 374-381. doi: 10.1038/nrendo.2009.106 PMID: 19488073
  7. Stratakis, C.A.; Chrousos, G.P. Neuroendocrinology and pathophysiology of the stress system. Ann. N. Y. Acad. Sci., 1995, 771(1 Stress), 1-18. doi: 10.1111/j.1749-6632.1995.tb44666.x PMID: 8597390
  8. Gold, P.W. The organization of the stress system and its dysregulation in depressive illness. Mol. Psychiatry, 2015, 20(1), 32-47. doi: 10.1038/mp.2014.163 PMID: 25486982
  9. Kousta, S. Mapping the structural and functional architecture of the brain. Trends Cogn. Sci., 2013, 17(12), 595. doi: 10.1016/j.tics.2013.10.009
  10. Baliyan, V.; Das, C.J.; Sharma, R.; Gupta, A.K. Diffusion weighted imaging: Technique and applications. World J. Radiol., 2016, 8(9), 785-798. doi: 10.4329/wjr.v8.i9.785 PMID: 27721941
  11. Glover, G.H. Overview of functional magnetic resonance imaging. Neurosurg. Clin. N. Am., 2011, 22(2), 133-139. vii. doi: 10.1016/j.nec.2010.11.001 PMID: 21435566
  12. Uddin, L.Q. Complex relationships between structural and functional brain connectivity. Trends Cogn. Sci., 2013, 17(12), 600-602. doi: 10.1016/j.tics.2013.09.011 PMID: 24094797
  13. Le Bihan, D.; Breton, E.; Lallemand, D.; Grenier, P.; Cabanis, E.; Laval-Jeantet, M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology, 1986, 161(2), 401-407. doi: 10.1148/radiology.161.2.3763909 PMID: 3763909
  14. Biswal, B.; Zerrin Yetkin, F.; Haughton, V.M.; Hyde, J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar mri. Magn. Reson. Med., 1995, 34(4), 537-541. doi: 10.1002/mrm.1910340409 PMID: 8524021
  15. Chang, C.; Glover, G.H. Time–frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage, 2010, 50(1), 81-98. doi: 10.1016/j.neuroimage.2009.12.011 PMID: 20006716
  16. Fox, M.D.; Raichle, M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci., 2007, 8(9), 700-711. doi: 10.1038/nrn2201 PMID: 17704812
  17. Borogovac, A.; Asllani, I. Arterial Spin Labeling (ASL) fMRI: advantages, theoretical constrains, and experimental challenges in neurosciences. Int. J. Biomed. Imaging, 2012, 2012, 818456. PMID: 22966219
  18. Liégeois, R.; Li, J.; Kong, R.; Orban, C.; Van De Ville, D.; Ge, T.; Sabuncu, M.R.; Yeo, B.T.T. Resting brain dynamics at different timescales capture distinct aspects of human behavior. Nat. Commun., 2019, 10(1), 2317. doi: 10.1038/s41467-019-10317-7 PMID: 31127095
  19. Zhang, S.; Li, X.; Lv, J.; Jiang, X.; Guo, L.; Liu, T. Characterizing and differentiating task-based and resting state fMRI signals via two-stage sparse representations. Brain Imaging Behav., 2016, 10(1), 21-32. doi: 10.1007/s11682-015-9359-7 PMID: 25732072
  20. Logothetis, N.K. What we can do and what we cannot do with fMRI. Nature, 2008, 453(7197), 869-878. doi: 10.1038/nature06976 PMID: 18548064
  21. Patanaik, A.; Tandi, J.; Ong, J.L.; Wang, C.; Zhou, J.; Chee, M.W.L. Dynamic functional connectivity and its behavioral correlates beyond vigilance. Neuroimage, 2018, 177, 1-10. doi: 10.1016/j.neuroimage.2018.04.049 PMID: 29704612
  22. Honey, C.J.; Sporns, O.; Cammoun, L.; Gigandet, X.; Thiran, J.P.; Meuli, R.; Hagmann, P. Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl. Acad. Sci. USA, 2009, 106(6), 2035-2040. doi: 10.1073/pnas.0811168106 PMID: 19188601
  23. Allen, E.A.; Damaraju, E.; Plis, S.M.; Erhardt, E.B.; Eichele, T.; Calhoun, V.D. Tracking whole-brain connectivity dynamics in the resting state. Cereb. Cortex, 2014, 24(3), 663-676. doi: 10.1093/cercor/bhs352 PMID: 23146964
  24. Zhang, X.; Huettel, S.A.; Mullette-Gillman, O.D.A.; Guo, H.; Wang, L. Exploring common changes after acute mental stress and acute tryptophan depletion: Resting-state fMRI studies. J. Psychiatr. Res., 2019, 113, 172-180. doi: 10.1016/j.jpsychires.2019.03.025 PMID: 30959228
  25. Pan, J.; Zhan, L.; Hu, C.; Yang, J.; Wang, C.; Gu, L.; Zhong, S.; Huang, Y.; Wu, Q.; Xie, X.; Chen, Q.; Zhou, H.; Huang, M.; Wu, X. Emotion regulation and complex brain networks: association between expressive suppression and efficiency in the fronto-parietal network and default-mode network. Front. Hum. Neurosci., 2018, 12, 70. doi: 10.3389/fnhum.2018.00070 PMID: 29662443
  26. Barch, D.M. Brain network interactions in health and disease. Trends Cogn. Sci., 2013, 17(12), 603-605. doi: 10.1016/j.tics.2013.09.004 PMID: 24080424
  27. Menon, V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci., 2011, 15(10), 483-506. doi: 10.1016/j.tics.2011.08.003 PMID: 21908230
  28. Zhang, W.; Hashemi, M.M.; Kaldewaij, R.; Koch, S.B.J.; Beckmann, C.; Klumpers, F.; Roelofs, K. Acute stress alters the ‘default’ brain processing. Neuroimage, 2019, 189, 870-877. doi: 10.1016/j.neuroimage.2019.01.063 PMID: 30703518
  29. Teng, J.; Ong, J.L.; Patanaik, A.; Tandi, J.; Zhou, J.H.; Chee, M.W.L.; Lim, J. Vigilance declines following sleep deprivation are associated with two previously identified dynamic connectivity states. Neuroimage, 2019, 200, 382-390. doi: 10.1016/j.neuroimage.2019.07.004 PMID: 31276798
  30. Shapiro, S.L.; Carlson, L.E.; Astin, J.A.; Freedman, B. Mechanisms of mindfulness. J. Clin. Psychol., 2006, 62(3), 373-386. doi: 10.1002/jclp.20237 PMID: 16385481
  31. Kabat-Zinn, J. Full catastrophe living: using the wisdom of your body and mind to face stress, pain, and illness, 2009.
  32. Mooneyham, B.W.; Mrazek, M.D.; Mrazek, A.J.; Mrazek, K.L.; Phillips, D.T.; Schooler, J.W. States of mind: Characterizing the neural bases of focus and mind-wandering through dynamic functional connectivity. J. Cogn. Neurosci., 2017, 29(3), 495-506. doi: 10.1162/jocn_a_01066 PMID: 27779908
  33. Hsu, N.S.; Fang, H.Y.; David, K.K.; Gnadt, J.W.; Peng, G.C.Y.; Talley, E.M.; Ward, J.M.; Ngai, J.; Koroshetz, W.J. The promise of the BRAIN initiative: NIH strategies for understanding neural circuit function. Curr. Opin. Neurobiol., 2020, 65, 162-166. doi: 10.1016/j.conb.2020.10.008 PMID: 33279793
  34. Jadad, A.R.; Moore, R.A.; Carroll, D.; Jenkinson, C.; Reynolds, D.J.M.; Gavaghan, D.J.; McQuay, H.J. Assessing the quality of reports of randomized clinical trials: Is blinding necessary? Control. Clin. Trials, 1996, 17(1), 1-12. doi: 10.1016/0197-2456(95)00134-4 PMID: 8721797
  35. Sinha, R.; Lacadie, C.; Skudlarski, P.; Wexler, B. Neural circuits underlying emotional distress in humans. Ann. N. Y. Acad. Sci., 2004, 1032(1), 254-257. doi: 10.1196/annals.1314.032 PMID: 15677422
  36. Wang, J.; Rao, H.; Wetmore, G.S.; Furlan, P.M.; Korczykowski, M.; Dinges, D.F.; Detre, J.A. Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc. Natl. Acad. Sci. USA, 2005, 102(49), 17804-17809. doi: 10.1073/pnas.0503082102 PMID: 16306271
  37. Veer, I.M.; Oei, N.Y.L.; Spinhoven, P.; van Buchem, M.A.; Elzinga, B.M.; Rombouts, S.A.R.B. Beyond acute social stress: Increased functional connectivity between amygdala and cortical midline structures. Neuroimage, 2011, 57(4), 1534-1541. doi: 10.1016/j.neuroimage.2011.05.074 PMID: 21664280
  38. Henckens, M.J.A.G.; van Wingen, G.A.; Joëls, M.; Fernández, G. Corticosteroid induced decoupling of the amygdala in men. Cereb. Cortex, 2012, 22(10), 2336-2345. doi: 10.1093/cercor/bhr313 PMID: 22079927
  39. Qin, S.; Hermans, E.J.; van Marle, H.J.F.; Fernández, G. Understanding low reliability of memories for neutral information encoded under stress: alterations in memory-related activation in the hippocampus and midbrain. J. Neurosci., 2012, 32(12), 4032-4041. doi: 10.1523/JNEUROSCI.3101-11.2012 PMID: 22442069
  40. Schwabe, L.; Tegenthoff, M.; Höffken, O.; Wolf, O.T. Mineralocorticoid receptor blockade prevents stress-induced modulation of multiple memory systems in the human brain. Biol. Psychiatry, 2013, 74(11), 801-808. doi: 10.1016/j.biopsych.2013.06.001 PMID: 23871473
  41. Gathmann, B.; Schulte, F.P.; Maderwald, S.; Pawlikowski, M.; Starcke, K.; Schäfer, L.C.; Schöler, T.; Wolf, O.T.; Brand, M. Stress and decision making: neural correlates of the interaction between stress, executive functions, and decision making under risk. Exp. Brain Res., 2014, 232(3), 957-973. doi: 10.1007/s00221-013-3808-6 PMID: 24408441
  42. Oei, N.Y.L.; Both, S.; van Heemst, D.; van der Grond, J. Acute stress-induced cortisol elevations mediate reward system activity during subconscious processing of sexual stimuli. Psychoneuroendocrinology, 2014, 39, 111-120. doi: 10.1016/j.psyneuen.2013.10.005 PMID: 24275010
  43. Grimm, S.; Pestke, K.; Feeser, M.; Aust, S.; Weigand, A.; Wang, J.; Wingenfeld, K.; Pruessner, J.C.; La Marca, R.; Böker, H.; Bajbouj, M. Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress. Soc. Cogn. Affect. Neurosci., 2014, 9(11), 1828-1835. doi: 10.1093/scan/nsu020 PMID: 24478326
  44. Fan, Y.; Pestke, K.; Feeser, M.; Aust, S.; Pruessner, J.C.; Böker, H.; Bajbouj, M.; Grimm, S. Amygdala-hippocampal connectivity changes during acute psychosocial stress: Joint effect of early life stress and oxytocin. Neuropsychopharmacology, 2015, 40(12), 2736-2744. doi: 10.1038/npp.2015.123 PMID: 25924202
  45. Vogel, S.; Klumpers, F.; Kroes, M.C.W.; Oplaat, K.T.; Krugers, H.J.; Oitzl, M.S.; Joëls, M.; Fernández, G. A stress-induced shift from trace to delay conditioning depends on the mineralocorticoid receptor. Biol. Psychiatry, 2015, 78(12), 830-839. doi: 10.1016/j.biopsych.2015.02.014 PMID: 25823790
  46. Khalili-Mahani, N.; Niesters, M.; van Osch, M.J.; Oitzl, M.; Veer, I.; de Rooij, M.; van Gerven, J.; van Buchem, M.A.; Beckmann, C.F.; Rombouts, S.A.R.B.; Dahan, A. Ketamine interactions with biomarkers of stress: A randomized placebo-controlled repeated measures resting-state fMRI and PCASL pilot study in healthy men. Neuroimage, 2015, 108, 396-409. doi: 10.1016/j.neuroimage.2014.12.050 PMID: 25554429
  47. Everaerd, D.; Klumpers, F.; van Wingen, G.; Tendolkar, I.; Fernández, G. Association between neuroticism and amygdala responsivity emerges under stressful conditions. Neuroimage, 2015, 112, 218-224. doi: 10.1016/j.neuroimage.2015.03.014 PMID: 25776217
  48. Maier, S.U.; Makwana, A.B.; Hare, T.A. Acute stress impairs self-control in goal-directed choice by altering multiple functional connections within the brain’s decision circuits. Neuron, 2015, 87(3), 621-631. doi: 10.1016/j.neuron.2015.07.005 PMID: 26247866
  49. Henckens, M.J.A.G.; Klumpers, F.; Everaerd, D.; Kooijman, S.C.; van Wingen, G.A.; Fernández, G. Interindividual differences in stress sensitivity: Basal and stress-induced cortisol levels differentially predict neural vigilance processing under stress. Soc. Cogn. Affect. Neurosci., 2016, 11(4), 663-673. doi: 10.1093/scan/nsv149 PMID: 26668010
  50. Vogel, S.; Klumpers, F.; Schröder, T.N.; Oplaat, K.T.; Krugers, H.J.; Oitzl, M.S.; Joëls, M.; Doeller, C.F.; Fernández, G. Stress induces a shift towards striatum-dependent stimulus-response learning via the mineralocorticoid receptor. Neuropsychopharmacology, 2017, 42(6), 1262-1271. doi: 10.1038/npp.2016.262 PMID: 27876790
  51. Gavelin, H.M.; Neely, A.S.; Andersson, M.; Eskilsson, T.; Järvholm, L.S.; Boraxbekk, C.J. Neural activation in stress-related exhaustion: Cross-sectional observations and interventional effects. Psychiatry Res. Neuroimaging, 2017, 269, 17-25. doi: 10.1016/j.pscychresns.2017.08.008 PMID: 28917154
  52. Kohn, N.; Hermans, E.J.; Fernández, G. Cognitive benefit and cost of acute stress is differentially modulated by individual brain state. Soc. Cogn. Affect. Neurosci., 2017, 12(7), 1179-1187. doi: 10.1093/scan/nsx043 PMID: 28402480
  53. Luo, Y.; Fernández, G.; Hermans, E.; Vogel, S.; Zhang, Y.; Li, H.; Klumpers, F. How acute stress may enhance subsequent memory for threat stimuli outside the focus of attention: DLPFC-amygdala decoupling. Neuroimage, 2018, 171, 311-322. doi: 10.1016/j.neuroimage.2018.01.010 PMID: 29329979
  54. Vogel, S.; Kluen, L.M.; Fernández, G.; Schwabe, L. Stress affects the neural ensemble for integrating new information and prior knowledge. Neuroimage, 2018, 173, 176-187. doi: 10.1016/j.neuroimage.2018.02.038 PMID: 29476913
  55. Chang, J.; Yu, R. Hippocampal connectivity in the aftermath of acute social stress. Neurobiol. Stress, 2019, 11, 100195. doi: 10.1016/j.ynstr.2019.100195 PMID: 31832509
  56. Maier, A.; Scheele, D.; Spengler, F.B.; Menba, T.; Mohr, F.; Güntürkün, O.; Stoffel-Wagner, B.; Kinfe, T.M.; Maier, W.; Khalsa, S.S.; Hurlemann, R. Oxytocin reduces a chemosensory-induced stress bias in social perception. Neuropsychopharmacology, 2019, 44(2), 281-288. doi: 10.1038/s41386-018-0063-3 PMID: 29703998
  57. van Leeuwen, J.M.C.; Vink, M.; Joëls, M.; Kahn, R.S.; Hermans, E.J.; Vinkers, C.H. Increased responses of the reward circuitry to positive task feedback following acute stress in healthy controls but not in siblings of schizophrenia patients. Neuroimage, 2019, 184, 547-554. doi: 10.1016/j.neuroimage.2018.09.051 PMID: 30243958
  58. Woodcock, E.A.; Greenwald, M.K.; Khatib, D.; Diwadkar, V.A.; Stanley, J.A. Pharmacological stress impairs working memory performance and attenuates dorsolateral prefrontal cortex glutamate modulation. Neuroimage, 2019, 186, 437-445. doi: 10.1016/j.neuroimage.2018.11.017 PMID: 30458306
  59. Reinelt, J.; Uhlig, M.; Müller, K.; Lauckner, M.E.; Kumral, D.; Schaare, H.L.; Baczkowski, B.M.; Babayan, A.; Erbey, M.; Roebbig, J.; Reiter, A.; Bae, Y.J.; Kratzsch, J.; Thiery, J.; Hendler, T.; Villringer, A.; Gaebler, M. Acute psychosocial stress alters thalamic network centrality. Neuroimage, 2019, 199, 680-690. doi: 10.1016/j.neuroimage.2019.06.005 PMID: 31173902
  60. Herrmann, L.; Vicheva, P.; Kasties, V.; Danyeli, L.V.; Szycik, G.R.; Denzel, D.; Fan, Y.; Meer, J.V.; Vester, J.C.; Eskoetter, H.; Schultz, M.; Walter, M. fMRI revealed reduced amygdala activation after Nx4 in mildly to moderately stressed healthy volunteers in a randomized, placebo-controlled, cross-over trial. Sci. Rep., 2020, 10(1), 3802. doi: 10.1038/s41598-020-60392-w PMID: 32123197
  61. Teng, J.; Massar, S.A.A.; Lim, J. Inter-relationships between changes in stress, mindfulness, and dynamic functional connectivity in response to a social stressor. Sci. Rep., 2022, 12(1), 2396. doi: 10.1038/s41598-022-06342-0 PMID: 35165343
  62. Corr, R.; Glier, S.; Bizzell, J.; Pelletier-Baldelli, A.; Campbell, A.; Killian-Farrell, C.; Belger, A. Triple network functional connectivity during acute stress in adolescents and the influence of polyvictimization. Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 2022, 7(9), 867-875. doi: 10.1016/j.bpsc.2022.03.003 PMID: 35292406
  63. Quabs, J.; Caspers, S.; Schöne, C.; Mohlberg, H.; Bludau, S.; Dickscheid, T.; Amunts, K. Cytoarchitecture, probability maps and segregation of the human insula. Neuroimage, 2022, 260, 119453. doi: 10.1016/j.neuroimage.2022.119453 PMID: 35809885
  64. Buckner, R.L.; Carroll, D.C. Self-projection and the brain. Trends Cogn. Sci., 2007, 11(2), 49-57. doi: 10.1016/j.tics.2006.11.004 PMID: 17188554
  65. Bilevicius, E.; Smith, S.D.; Kornelsen, J. Resting-state network functional connectivity patterns associated with the mindful attention awareness scale. Brain Connect., 2018, 8(1), 40-48. doi: 10.1089/brain.2017.0520 PMID: 29130326
  66. Doll, A.; Hölzel, B.K.; Boucard, C.C.; Wohlschläger, A.M.; Sorg, C. Mindfulness is associated with intrinsic functional connectivity between default mode and salience networks. Front. Hum. Neurosci., 2015, 9, 461. doi: 10.3389/fnhum.2015.00461 PMID: 26379526
  67. Lim, J.; Teng, J.; Patanaik, A.; Tandi, J.; Massar, S.A.A. Dynamic functional connectivity markers of objective trait mindfulness. Neuroimage, 2018, 176, 193-202. doi: 10.1016/j.neuroimage.2018.04.056 PMID: 29709625
  68. Cannon, W.B. The wisdom of the body; W.W. Norton & Company: New York, 1932. doi: 10.1097/00000441-193212000-00028
  69. Gianaros, P.J.; Derbtshire, S.W.G.; May, J.C.; Siegle, G.J.; Gamalo, M.A.; Jennings, J.R. Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology, 2005, 42(6), 627-635. doi: 10.1111/j.1469-8986.2005.00366.x PMID: 16364058
  70. Pace, T.W.W.; Gaylord, R.I.; Jarvis, E.; Girotti, M.; Spencer, R.L. Differential glucocorticoid effects on stress-induced gene expression in the paraventricular nucleus of the hypothalamus and ACTH secretion in the rat. Stress, 2009, 12(5), 400-411. doi: 10.1080/10253890802530730 PMID: 19065454
  71. Cunningham-Bussel, A.C.; Root, J.C.; Butler, T.; Tuescher, O.; Pan, H.; Epstein, J.; Weisholtz, D.S.; Pavony, M.; Silverman, M.E.; Goldstein, M.S.; Altemus, M.; Cloitre, M.; LeDoux, J.; McEwen, B.; Stern, E.; Silbersweig, D. Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli. Psychoneuroendocrinology, 2009, 34(5), 694-704. doi: 10.1016/j.psyneuen.2008.11.011 PMID: 19135805
  72. Qin, C.; Li, J.; Tang, K. The paraventricular nucleus of the hypothalamus: development, function, and human diseases. Endocrinology, 2018, 159(9), 3458-3472. doi: 10.1210/en.2018-00453 PMID: 30052854
  73. Ma, S.; Morilak, D.A. Norepinephrine release in medial amygdala facilitates activation of the hypothalamic-pituitary-adrenal axis in response to acute immobilisation stress. J. Neuroendocrinol., 2005, 17(1), 22-28. doi: 10.1111/j.1365-2826.2005.01279.x PMID: 15720472
  74. Aguilera, G. Regulation of the hypothalamic-pituitary-adrenal axis by neuropeptides. Horm. Mol. Biol. Clin. Investig., 2011, 7(2), 327-336. doi: 10.1515/HMBCI.2011.123 PMID: 25961271
  75. LeDoux, J. The amygdala. Curr. Biol., 2007, 17(20), R868-R874. doi: 10.1016/j.cub.2007.08.005 PMID: 17956742
  76. Uddin, L.Q. Salience processing and insular cortical function and dysfunction. Nat. Rev. Neurosci., 2015, 16(1), 55-61. doi: 10.1038/nrn3857 PMID: 25406711
  77. Sandi, C. Stress and cognition. Wiley Interdiscip. Rev. Cogn. Sci., 2013, 4(3), 245-261. doi: 10.1002/wcs.1222 PMID: 26304203
  78. Engert, V.; Kok, B.E.; Papassotiriou, I.; Chrousos, G.P.; Singer, T. Specific reduction in cortisol stress reactivity after social but not attention-based mental training. Sci. Adv., 2017, 3(10), e1700495. doi: 10.1126/sciadv.1700495 PMID: 28983508

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers