Stress-induced activation of the HPA axis predicts connectivity between subgenual cingulate and salience network during rest in adolescents

Journal of Child Psychology and Psychiatry and Allied Disciplines

Volumn 52, Issue 10, 2011, Pages 1026-1034

  Thomason, Moriah E ^a,b   Hamilton, J Paul ^c   Gotlib, Ian H ^c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

adolescents; connectivity; fMRI; HPA axis; Resting state; salience network; stress; subgenual cingulate

Indexed keywords

DIAGNOSTIC AGENT; HYDROCORTISONE;

ADOLESCENT; ARTICLE; CHILD; CINGULATE GYRUS; HUMAN; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; NERVE CELL NETWORK; PHYSIOLOGY; PREFRONTAL CORTEX; REST; SECRETION;

ADOLESCENT; CHILD; GYRUS CINGULI; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NERVE NET; PITUITARY-ADRENAL SYSTEM; PREFRONTAL CORTEX; REST; STRESS, PSYCHOLOGICAL;

EID: 80052518577     PISSN: 00219630     EISSN: 14697610     Source Type: Journal    
DOI: 10.1111/j.1469-7610.2011.02422.x     Document Type: Review

References (55)

1. Buchanan, T.W., Driscoll, D., Mowrer, S.M., Sollers, J.J. III, Thayer, J.F., Kirschbaum, C., &, Tranel, D., (2010). Medial prefrontal cortex damage affects physiological and psychological stress responses differently in men and women. Psychoneuroendocrinology, 35, 56-66.
2. Calhoun, V.D., Adali, T., Pearlson, G.D., &, Pekar, J.J., (2001). A method for making group inferences from functional MRI data using independent component analysis. Human Brain Mapping, 14, 140-151. (Pubitemid 33032347)
3. Chua, P., Krams, M., Toni, I., Passingham, R., &, Dolan, R., (1999). A functional anatomy of anticipatory anxiety. Neuroimage, 9, 563-571. (Pubitemid 29369882)
4. Critchley, H.D., (2005). Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493, 154-166. (Pubitemid 41636198)
5. Cunningham, M.G., Bhattacharyya, S., &, Benes, F.M., (2002). Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. Journal of Comparative Neurology, 453, 116-130. (Pubitemid 35155051)
6. Damasio, A.R., Grabowski, T.J., Bechara, A., Damasio, H., Ponto, L.L., Parvizi, J., &, Hichwa, R.D., (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience, 3, 1049-1056.
7. Eatough, E.M., Shirtcliff, E.A., Hanson, J.L., &, Pollak, S.D., (2009). Hormonal reactivity to MRI scanning in adolescents. Psychoneuroendocrinology, 34, 1242-1246.
8. Ewart, C., Jorgensen, R., Suchday, S., Chen, E., &, Matthews, K., (2002). Measuring stress resilience and coping in vulnerable youth: The social competence interview. Psychological Assessment, 14, 339-352. (Pubitemid 34913390)
9. Fair, D.A., Bathula, D., Mills, K.L., Dias, T.G., Blythe, M.S., Zhang, D., Snyder, A.Z., Raichle, M.E., Stevens, A.A., Nigg, J.T., &, Nagel, B.J., (2010). Maturing thalamocortical functional connectivity across development. Frontiers in Systems Neuroscience, 4, 10.
10. Fair, D.A., Dosenbach, N.U.F., Church, J.A., Cohen, A.L., Brahmbhatt, S., Miezin, F.M., Barch, D.M., Raichle, M.E., Petersen, S.E., &, Schlaggar, B.L., (2007). Development of distinct control networks through segregation and integration. Proceedings of the National Academy of Sciences of the United States of America, 104, 13507-13512. (Pubitemid 47293975)
11. Figueiredo, H.F., Bruestle, A., Bodie, B., Dolgas, C.M., &, Herman, J.P., (2003). The medial prefrontal cortex differentially regulates stress-induced c-fos expression in the forebrain depending on type of stressor. European Journal of Neuroscience, 18, 2357-2364. (Pubitemid 38117410)
12. Geller, B., Williams, M., Zimerman, B., &, Frazier, J., (1996). WASH-U-KSADS (Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia). St Louis, MO: Washington University.
13. Geller, B., Zimerman, B., Williams, M., Bolhofner, K., Craney, J.L., Delbello, M.P., &, Soutullo, C., (2001). Reliability of the Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia (WASH-U-KSADS) mania and rapid cycling sections. Journal of the American Academy of Child and Adolescent Psychiatry, 40, 450-455. (Pubitemid 32242529)
14. Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., Paus, T., Evans, A.C., &, Rapoport, J.L., (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861-863. (Pubitemid 30602596)
15. Gotlib, I.H., &, Hamilton, J.P., (2008). Neuroimaging and depression: Current status and unresolved issues. Current Directions in Psychological Science, 17, 159-163.
16. Gotlib, I.H., Joormann, J., Minor, K.L., &, Hallmayer, J., (2008). HPA axis reactivity: A mechanism underlying the associations among 5-HTTLPR, stress, and depression. Biological Psychiatry, 63, 847-851. (Pubitemid 351458452)
17. Gotlib, I.H., Sivers, H., Gabrieli, J.D., Hallmayer, J., Whitfield-Gabrieli, S., Goldin, P., Minor, K.L., &, Canli, T., (2005). Neuroreport, 16, 1731-1734.
18. Greicius, M.D., Flores, B.H., Menon, V., Glover, G.H., Solvason, H.B., Kenna, H., Reiss, A.L., &, Schatzberg, A.F., (2007). Resting-state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry, 62, 429-437. (Pubitemid 47284017)
19. Grinband, J., Hirsch, J., &, Ferrera, V.P., (2006). A neural representation of categorization uncertainty in the human brain. Neuron, 49, 757-763. (Pubitemid 43290134)
20. Gross, C., &, Hen, R., (2004). The developmental origins of anxiety. Nature Reviews. Neuroscience, 5, 545-552. (Pubitemid 38868550)
21. Hamilton, J.P., Furman, D.J., Chang, C., Thomason, M.E., Dennis, E., &, Gotlib, I.H., (in press). Default-mode and task-positive network activity in major depressive disorder: Implications for adaptive and maladaptive rumination. Biological Psychiatry, 62, 429-437.
22. Huttenlocher, P., (1979). Synaptic density in human frontal-cortex- Developmental changes and effects of aging. Brain Research, 163, 195-205. (Pubitemid 9138619)
23. Jahn, A.L., Fox, A.S., Abercrombie, H.C., Shelton, S.E., Oakes, T.R., Davidson, R.J., &, Kalin, N.H., (2010). Subgenual prefrontal cortex activity predicts individual differences in hypothalamic-pituitary-adrenal activity across different contexts. Biological Psychiatry, 67, 175-181.
24. Joormann, J., Talbot, L., &, Gotlib, I.H., (2007). Biased processing of emotional information in girls at risk for depression. Journal of Abnormal Psychology, 116, 135-143. (Pubitemid 46328604)
25. Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., Williamson, D., &, Ryan, N., (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 980-988. (Pubitemid 27272932)
26. Koch, K., Pauly, K., Kellermann, T., Seiferth, N.Y., Reske, M., Backes, V., Stocker, T., Shah, N.J., Amunts, K., Kircher, T., Schneider, F., &, Habel, U., (2007). Gender differences in the cognitive control of emotion: An fMRI study. Neuropsychologia, 45, 2744-2754. (Pubitemid 47176582)
27. Kovacs, M., Joormann, J., &, Gotlib, I.H., (2008). Emotion (Dys)regulation and links to depressive disorders. Child Development Perspectives, 2, 149-155.
28. Liberzon, I., King, A.P., Britton, J.C., Phan, K.L., Abelson, J.L., &, Taylor, S.F., (2007). Paralimbic and medial prefrontal cortical involvement in neuroendocrine responses to traumatic stimuli. American Journal of Psychiatry, 164, 1250-1258. (Pubitemid 47292415)
29. Liotti, M., Mayberg, H.S., Mcginnis, S., Brannan, S.L., &, Jerabek, P., (2002). Unmasking disease-specific cerebral blood flow abnormalities: Mood challenge in patients with remitted unipolar depression. American Journal of Psychiatry, 159, 1830-1840. (Pubitemid 35283247)
30. Maddock, R.J., Garrett, A.S., &, Buonocore, M.H., (2003). Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Human Brain Mapping, 18, 30-41. (Pubitemid 35462614)
31. Mayberg, H.S., (2003). Positron emission tomography imaging in depression: A neural systems perspective. Neuroimaging Clinics of North America, 13, 805-815. (Pubitemid 37445057)
32. Mayberg, H.S., Liotti, M., Brannan, S.K., Mcginnis, S., Mahurin, R.K., Jerabek, P.A., Silva, J.A., Tekell, J.L., Martin, C.C., Lancaster, J.L., &, Fox, P.T., (1999). Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. American Journal of Psychiatry, 156, 675-682. (Pubitemid 29220063)
33. Mayberg, H.S., Lozano, A.M., Voon, V., Mcneely, H.E., Seminowicz, D., Hamani, C., Schwalb, J.M., &, Kennedy, S.H., (2005). Deep brain stimulation for treatment-resistant depression. Neuron, 45, 651-660. (Pubitemid 40320700)
34. Menon, V., Adleman, N.E., White, C.D., Glover, G.H., &, Reiss, A.L., (2001). Error-related brain activation during a Go/NoGo response inhibition task. Human Brain Mapping, 12, 131-143. (Pubitemid 32186917)
35. Muehlhan, M., Lueken, U., Wittchen, H.U., &, Kirschbaum, C., (2011). The scanner as a stressor: Evidence from subjective and neuroendocrine stress parameters in the time course of a functional magnetic resonance imaging session. International Journal of Psychophysiology, 79, 118-126.
36. Peyron, R., Laurent, B., &, Garcia-Larrea, L., (2000). Functional imaging of brain responses to pain. A review and meta-analysis. Clinical Neurophysiology, 30, 263-288.
37. Pfefferbaum, A., Mathalon, D.H., Sullivan, E.V., Rawles, J.M., Zipursky, R.B., &, Lim, K.O., (1994). A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Archives of Neurology, 51, 874-887. (Pubitemid 24286042)
38. Pruessner, J.C., Dedovic, K., Pruessner, M., Lord, C., Buss, C., Collins, L., Dagher, A., &, Lupien, S.J., (2010). Stress regulation in the central nervous system: Evidence from structural and functional neuroimaging studies in human populations-2008 Curt Richter Award Winner. Psychoneuroendocrinology, 35, 179-191.
39. Pruessner, J.C., Kirschbaum, C., Meinlschmid, G., &, Hellhammer, D.H., (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916-931. (Pubitemid 36936799)
40. Seeley, W.W., Menon, V., Schatzberg, A.F., Keller, J., Glover, G.H., Kenna, H., Reiss, A.L., &, Greicius, M.D., (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27, 2349-2356. (Pubitemid 46340968)
41. Seminowicz, D.A., Mayberg, H.S., Mcintosh, A.R., Goldapple, K., Kennedy, S., Segal, Z., &, Rafi-Tari, S., (2004). Limbic-frontal circuitry in major depression: A path modeling metanalysis. Neuroimage, 22, 409-418. (Pubitemid 38515850)
42. Sowell, E.R., Thompson, P.M., Holmes, C.J., Jernigan, T.L., &, Toga, A.W., (1999). In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nature Neuroscience, 2, 859-861. (Pubitemid 30602595)
43. Sowell, E.R., Thompson, P.M., Leonard, C.M., Welcome, S.E., Kan, E., &, Toga, A.W., (2004). Longitudinal mapping of cortical thickness and brain growth in normal children. Journal of Neuroscience, 24, 8223-8231. (Pubitemid 39280801)
44. Sowell, E.R., Thompson, P.M., &, Toga, A.W., (2004). Mapping changes in the human cortex throughout the span of life. Neuroscientist, 10, 372-392. (Pubitemid 38971216)
45. Sridharan, D., Levitin, D.J., &, Menon, V., (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences of the United States of America, 105, 12569-12574.
46. Stevens, M.C., Pearlson, G.D., &, Calhoun, V.D., (2009). Changes in the interaction of resting-state neural networks from adolescence to adulthood. Human Brain Mapping, 30, 2356-2366.
47. Taylor, K.S., Seminowicz, D.A., &, Davis, K.D., (2009). Two systems of resting state connectivity between the insula and cingulate cortex. Human Brain Mapping, 30, 2731-2745.
48. Tchiteya, B.M., Lecours, A.R., Elie, R., &, Lupien, S.J., (2003). Impact of a unilateral brain lesion on cortisol secretion and emotional state: Anterior/posterior dissociation in humans. Psychoneuroendocrinology, 28, 674-686. (Pubitemid 36519659)
49. Thomason, M.E., Burrows, B.E., Gabrieli, J.D., &, Glover, G.H., (2005). Breath holding reveals differences in fMRI BOLD signal in children and adults. Neuroimage, 25, 824-837. (Pubitemid 40461721)
50. Thomason, M.E., Dennis, E.L., Joshi, A.A., Joshi, S.H., Dinov, I.D., Chang, C., Henry, M.L., Johnson, R.F., Thompson, P.M., Toga, A.W., Glover, G.H., Van Horn, J.D., &, Gotlib, I.H., (2011). Resting-state fMRI can reliably map neural networks in children. Neuroimage, 55, 165-175.
51. Thomason, M.E., &, Thompson, P.M., (2011). Diffusion imaging, white matter and psychopathology. In:, S. Nolen-Hoeksma, T.D. Cannon, &, T. Widiger, (Eds.), Annual review of clinical psychology, (Vol. 7) (pp. 63-85). Palo Alto, CA: Annual Reviews.
52. Uddin, L., Supekar, K., &, Menon, V., (2010). Typical and atypical development of functional human brain networks: Insights from resting-state fMRI. Frontiers in Systems Neuroscience, 4, 1-12.
53. Wager, T.D., Waugh, C.E., Lindquist, M., Noll, D.C., Fredrickson, B.L., &, Taylor, S.F., (2009). Brain mediators of cardiovascular responses to social threat: Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage, 47, 821-835.
54. White, T.P., Joseph, V., Francis, S.T., &, Liddle, P.F., (2010). Aberrant salience network (bilateral insula and anterior cingulate cortex) connectivity during information processing in schizophrenia. Schizophrenia Research, 123, 105-115.
55. Zald, D.H., Mattson, D.L., &, Pardo, J.V., (2002). Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. Proceedings of the National Academy of Sciences of the United States of America, 99, 2450-2454. (Pubitemid 34169081)