The developmental relationship between DHEA and visual attention is mediated by structural plasticity of cortico-amygdalar networks

Psychoneuroendocrinology

Volumn 70, Issue , 2016, Pages 122-133

  Nguyen, Tuong Vi ^a   Gower, Patricia ^b   Albaugh, Matthew D ^c   Botteron, Kelly N ^d,e   Hudziak, James J ^c,e   Fonov, Vladimir S ^f   Collins, Louis ^f   Ducharme, Simon ^f,g   McCracken, James T ^e,h  

^a ROYAL VICTORIA HOSPITAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF VERMONT   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Brain Development Cooperative Group   (Canada)

^f MCGILL UNIVERSITY   (Canada)

^g MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adolescents; Adrenarche; Androgen; Human brain; Visual awareness; Visuo motor dexterity

Indexed keywords

ESTRADIOL; PRASTERONE; TESTOSTERONE;

ADOLESCENCE; ADOLESCENT; ADULT; AMYGDALA; ANTERIOR CINGULATE; ARTICLE; ATTENTION; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SIZE; CHILD; CHILDHOOD; CORTICAL THICKNESS (BRAIN); FEMALE; HUMAN; MALE; MORPHOLOGY; NERVE CELL PLASTICITY; OCCIPITAL LOBE; PARIETAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUBERTY; SENSORIMOTOR FUNCTION; VISION; VISUAL ATTENTION; ADRENARCHE; CHILD DEVELOPMENT; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; LONGITUDINAL STUDY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

ADOLESCENT; ADRENARCHE; AMYGDALA; ATTENTION; CEREBRAL CORTEX; CHILD; CHILD DEVELOPMENT; DEHYDROEPIANDROSTERONE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LONGITUDINAL STUDIES; MALE; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; VISION, OCULAR; YOUNG ADULT;

EID: 84969849665     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2016.05.003     Document Type: Article

References (78)

1. Achenbach T.M., Rescorla L. Manual for the ASEBA: School-Age Forms and Profiles 2001, University of Vermont, Department of Psychiatry, Burlington (VT).
2. Achenbach T.M., Rescorla L.A. Manual for the ASEBA School-Age Forms & Profiles 2001, University of Vermont, Research Center for Children, Youth, and Families, Burlington VT.
3. Achenbach T.M. Manual for the Child Behavior Checklist 4-18 and 1991 Profile 1991, University of Vermont, Department of Psychiatry, Burlington VT.
4. Achenbach T.M. Manual for the Young Adult Self-Report and Young Adult Behavior Checklist 1997, University of Vermont, Department of Psychiatry, Burlington (VT).
5. Adams J.B. Control of secretion and the function of C19-delta 5-steroids of the human adrenal gland. Mol. Cell. Endocrinol. 1985, 41:1-17.
6. Aebi M., Winkler Metzke C., Steinhausen H.C. Accuracy of the DSM-oriented attention problem scale of the child behavior checklist in diagnosing attention-deficit hyperactivity disorder. J. Atten. Disord. 2010, 13:454-463.
7. Albaugh M.D., Ducharme S., Collins D.L., Botteron K.N., Althoff R.R., Evans A.C., Karama S., Hudziak J.J. Evidence for a cerebral cortical thickness network anti-correlated with amygdalar volume in healthy youths: implications for the neural substrates of emotion regulation. Neuroimage 2013, 71:42-49.
8. Amaral D.G., Price J.L., Pitkanen A., Carmichael S.T. Anatomical organization of the primate amygdaloid complex. The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction 1992, Wiley-Liss, New York. J. Aggleton (Ed.).
9. Baulieu E.E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 1998, 23:963-987.
10. Brambilla D.J., Matsumoto A.M., Araujo A.B., McKinlay J.B. The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in mem. J. Clin. Endocrinol. Metabol. 2009, 94:907-913.
11. Butler P.D., Zemon V., Schechter I., Saperstein A.M., Hoptman M.J., Lim K.O., Revheim N., Silipo G., Javitt D.C. Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch. Gen. Psychiatry 2005, 62:495-504.
12. Campbell B.C. Adrenarche and middle childhood. Hum. Nat. 2011, 22:327-349.
13. Casey B.J., Jones R.M. Neurobiology of the adolescent brain and behavior: implications for substance use disorders. J. Am. Acad. Child Adolesc. Psychiatry 2010, 49:1189-1201.
14. Collins D.L., Evans A.C. Animal: validation and applications of nonlinear registration-Based segmentation. Int. J. Pattern Recognit. Artif. Intell. 1997, 11:1271-1294.
15. Collins D.L., Pruessner J.C. Towards accurate, automatic segmentation of the hippocampus and amygdala from MRI by augmenting ANIMAL with a template library and label fusion. Neuroimage 2010, 52:1355-1366.
16. Compagnone N.A., Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 2000, 21:1-56.
17. Cyr M., Landry M., Di Paolo T. Modulation by estrogen-receptor directed drugs of 5-hydroxytryptamine-2A receptors in rat brain. Neuropsychopharmacology 2000, 23:69-78.
18. Dabbs J.M. Salivary testosterone measurements: reliability across hours, days, and weeks. Physiol. Behav. 1990, 48:83-86.
19. Davis S.R., Shah S.M., McKenzie D.P., Kulkarni J., Davison S.L., Bell R.J. Dehydroepiandrosterone sulfate levels are associated with more favorable cognitive function in women. J. Clin. Endocrinol. Metab. 2008, 93:801-808.
20. Dolcos F., McCarthy G. Brain systems mediating cognitive interference by emotional distraction. J. Neurosci. 2006, 26:2072-2079.
21. Etkin A., Egner T., Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn. Sci. 2011, 15:85-93.
22. Evans A.C. The NIH MRI study of normal brain development. Neuroimage 2006, 30:184-202.
23. Fonda S.J., Bertrand R., O'Donnell A., Longcope C., McKinlay J.B. Age, hormones, and cognitive functioning among middle-aged and elderly men: cross-sectional evidence from the Massachusetts Male Aging Study. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:385-390.
24. Freese J.L., Amaral D.G. The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey. J. Comp. Neurol. 2005, 486:295-317.
25. Gabard-Durnam L.J., Flannery J., Goff B., Gee D.G., Humphreys K.L., Telzer E., Hare T., Tottenham N. The development of human amygdala functional connectivity at rest from 4 to 23 years: a cross-sectional study. Neuroimage 2014, 95:193-207.
26. Gee D.G., Humphreys K.L., Flannery J., Goff B., Telzer E.H., Shapiro M., Hare T.A., Bookheimer S.Y., Tottenham N. A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J. Neurosci. 2013, 33:4584-4593.
27. Goodale M.A., Milner A.D. Separate visual pathways for perception and action. Trends Neurosci. 1992, 15:20-25.
28. Granger D.A., Shirtcliff E.A., Booth A., Kivlighan K.T., Schwartz E.B. The trouble with salivary testosterone. Psychoneuroendocrinology 2004, 29:1229-1240.
29. Graydon F.X., Friston K.J., Thomas C.G., Brooks V.B., Menon R.S. Learning-related fMRI activation associated with a rotational visuo-motor transformation. Brain Res. Cogn. Brain Res. 2005, 22:373-383.
30. Hayes A.F. Beyond Baron and Kenny: statistical mediation analysis in the new millennium. Commun. Monogr. 2009, 76:408-420.
31. Herting M.M., Gautam P., Spielberg J.M., Dahl R.E., Sowell E.R. A longitudinal study: changes in cortical thickness and surface area during pubertal maturation. PLoS One 2015, 10:e0119774.
32. Kancheva R., Hill M., Novák Z., Chrastina J., Kancheva L., Stárka L. Neuroactive steroids in periphery and cerebrospinal fluid. Neuroscience 2011, 191:22-27.
33. Khan-Dawood F.S., Choe J.K., Dawood M.Y. Salivary and plasma bound and free testosterone in men and women. Am. J. Obstet. Gynecol. 1984, 148:441-445.
34. Kim M.J., Loucks R.A., Palmer A.L., Brown A.C., Solomon K.M., Marchante A.N., Whalen P.J. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav. Brain Res. 2011, 223:403-410.
35. Lee T.M.C., Cheung P.P. The relationship between visual-perception and attention in Chinese with schizophrenia. Schizophr. Res. 2005, 72:185-193.
36. Li Z., Cui S., Zhang Z., Zhou R., Ge Y., Sokabe M., Chen L. DHEA-neuroprotection and -neurotoxicity after transient cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 2008, 29:287-296.
37. Maninger N., Wolkowitz O.M., Reus V.I., Epel E.S., Mellon S.H. Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS). Front. Neuroendocrinol. 2009, 30:65-91.
38. Mishkin M., Ungerleider L.G. Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav. Brain Res. 1982, 6:57-77.
39. Morris J.S., DeGelder B., Weiskrantz L., Dolan R.J. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 2001, 124:1241-1252.
40. Musgrove D.R., Eberly L.E., Klimes-Dougan B., Basgoze Z., Thomas K.M., Mueller B.A., Houri A., Lim K.O., Cullen K.R. Impaired bottom-up effective connectivity between amygdala and subgenual anterior cingulate cortex in unmedicated adolescents with major depression: results from a dynamic causal modeling analysis. Brain Connect 2015.
41. Naert G., Maurice T., Tapia-Arancibia L., Givalois L. Neuroactive steroids modulate HPA axis activity and cerebral brain-derived neurotrophic factor (BDNF) protein levels in adult male rats. Psychoneuroendocrinology 2007, 32:1062-1078.
42. Nguyen T.V., McCracken J., Ducharme S., Botteron K.N., Mahabir M., Johnson W., Israel M., Evans A.C., Karama S. Testosterone-related cortical maturation across childhood and adolescence. Cereb. Cortex 2013, 23:1424-1432.
43. Nguyen T.V., McCracken J.T., Ducharme S., Cropp B.F., Botteron K.N., Evans A.C., Karama S. Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development. J. Neurosci. 2013, 33:10840-10848.
44. Park-Chung M., Malayev A., Purdy R.H., Gibbs T.T., Farb D.H. Sulfated and unsulfated steroids modulate gamma-aminobutyric acidA receptor function through distinct sites. Brain Res. 1999, 830:72-87.
45. Pasley B.N., Mayes L.C., Schultz R.T. Subcortical discrimination of unperceived objects during binocular rivalry. Neuron 2004, 42:163-172.
46. Patel G.H., Yang D., Jamerson E.C., Snyder L.H., Corbetta M., Ferrera V.P. Functional evolution of new and expanded attention networks in humans. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:9454-9459.
47. Pegna A.J., Khateb A., Lazeyras F., Seghier M.L. Discriminating emotional faces without primary visual cortices involves the right amygdala. Nat. Neurosci. 2005, 8:24-25.
48. Perlman S.B., Pelphrey K.A. Developing connections for affective regulation: age-related changes in emotional brain connectivity. J. Exp. Child Psychol. 2011, 108:607-620.
49. Pessoa L. On the relationship between emotion and cognition. Nat. Rev. Neurosci. 2008, 9:148-158.
50. Petersen A., Crockett L., Richards M., Boxer A. A self-report measure of pubertal status: reliability, validity, and initial norms. J. Youth Adolesc. 1988, 17:117-133.
51. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
52. Preuss T.M., Coleman G.Q. Human-specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb. Cortex 2002, 12:671-691.
53. Prouteau A., Verdoux H., Briand C., Lesage A., Lalonde P., Nicole L., Reirtharz D., Stip E. The crucial role of sustained attention in community functioning in outpatients with schizophrenia. Psychiatry Res. 2004, 129:171-177.
54. Pruessner J.C., Li L.M., Serles W., Pruessner M., Collins D.L., Kabani N., Lupien S., Evans A.C. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb. Cortex 2000, 10:433-442.
55. Pruessner J.C., Collins D.L., Pruessner M., Evans A.C. Age and gender predict volume decline in the anterior and posterior hippocampus in early adulthood. J. Neurosci. 2001, 21:194-200.
56. Raznahan A., Lerch Jason P., Lee N., Greenstein D., Wallace Gregory L., Stockman M., Clasen L., Shaw Phillip W., Giedd Jay N. Patterns of coordinated anatomical change in human cortical development: a longitudinal neuroimaging study of maturational coupling. Neuron 2011, 72:873-884.
57. Regelson W., Kalimi M. Dehydroepiandrosterone (Dhea) - the multifunctional steroid. 2. Effects on the Cns, cell-proliferation, metabolic and vascular, clinical and other effects - mechanism of action. Aging Clock 1994, 719:564-575.
58. Remer T., Boye K.R., Hartmann M.F., Wudy S.A. Urinary markers of adrenarche: reference values in healthy subjects, aged 3-18 years. J. Clin. Endocrinol. Metabol. 2005, 90:2015-2021.
59. Richards J.E. Cognitive Neuroscience of Attention: A Developmental Perspective 1998, Psychology Press.
60. Ritsner M.S., Gibel A., Ratner Y., Tsinovoy G., Strous R.D. Improvement of sustained attention and visual and movement skills, but not clinical symptoms, after dehydroepiandrosterone augmentation in schizophrenia-a randomized, double-blind, placebo-controlled, crossover trial. J. Clin. Psychopharmacol. 2006, 26:495-499.
61. Sah P., Faber E.S., Lopez De Armentia M., Power J. The amygdaloid complex: anatomy and physiology. Physiol. Rev. 2003, 83:803-834.
62. Sellers J.G., Mehl M.R., Josephs R.A. Hormones and personality: testosterone as a marker of individual differences. J. Res. Pers. 2007, 41:126-138.
63. Sripada R.K., Marx C.E., King A.P., Rajaram N., Garfinkel S.N., Abelson J.L., Liberzon I. DHEA enhances emotion regulation neurocircuits and modulates memory for emotional stimuli. Neuropsychopharmacology 2013, 38:1798-1807.
64. Sripada R.K., Welsh R.C., Marx C.E., Liberzon I. The neurosteroids allopregnanolone and dehydroepiandrosterone modulate resting-state amygdala connectivity. Hum. Brain Mapp. 2014, 35:3249-3261.
65. Stanczyk F.Z. Measurement of androgens in women. Semin. Reprod. Med. 2006, 24:78-85.
66. Stevens J.P. Applied Multivariate Statistics for the Social Sciences 2002, Erlbaum, Hillsdale, New Jersey. 4th ed.).
67. Strous R.D., Spivak B., Yoran-Hegesh R., Maayan R., Averbuch E., Kotler M., Mester R., Weizman A. Analysis of neurosteroid levels in attention deficit hyperactivity disorder. Int. J. Neuropsychopharmacol. 2001, 4:259-264.
68. Swartz J.R., Carrasco M., Wiggins J.L., Thomason M.E., Monk C.S. Age-related changes in the structure and function of prefrontal cortex-amygdala circuitry in children and adolescents: a multi-modal imaging approach. Neuroimage 2014, 86:212-220.
69. Troiani V., Schultz R.T. Amygdala, pulvinar, and inferior parietal cortex contribute to early processing of faces without awareness. Front. Hum. Neurosci. 2013, 7.
70. van Niekerk J.K., Huppert F.A., Herbert J. Salivary cortisol and DHEA: association with measures of cognition and well-being in normal older men, and effects of three months of DHEA supplementation. Psychoneuroendocrinology 2001, 26:591-612.
71. Vining R., McGinley R. The measurement of hormones in saliva: possibilities and pitfalls. J. Steroid Biochem. 1987, 27:81-94.
72. Vos M., Lauwers E., Verstreken P. Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease. Front. Synaptic Neurosci. 2010, 2:139.
73. Vuilleumier P., Armony J.L., Driver J., Dolan R.J. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat. Neurosci. 2003, 6:624-631.
74. Wechsler D. Wechsler Intelligence Scale for Children 1991, Psychological Corporation, New York.
75. Williams M.A., Morris A.P., McGlone F., Abbott D.F., Mattingley J.B. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J. Neurosci. 2004, 24:2898-2904.
76. Wolf O.T., Kudielka B.M., Hellhammer D.H., Hellhammer J., Kirschbaum C. Opposing effects of DHEA replacement in elderly subjects on declarative memory and attention after exposure to a laboratory stressor. Psychoneuroendocrinology 1998, 23:617-629.
77. Woodcock R.W., McGrew K.S., Mather N. Woodcock-Johnson III 2001, Riverside Publishing, Itasca, IL.
78. Worthman C.M., Stallings J.F., Hofman L.F. Sensitive salivary estradiol assay for monitoring ovarian function. Clin. Chem. 1990, 36:1769-1773.