Developmental investigation of fear-potentiated startle across puberty

Biological Psychology

Volumn 97, Issue 1, 2014, Pages 15-21

  Schmitz, Anja ^a   Grillon, Christian ^a   Avenevoli, Shelli ^a   Cui, Lihong ^a   Merikangas, Kathleen R ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Adolescence; Anxiety; Development; Fear potentiated startle; Puberty; Sex differences

Indexed keywords

ADOLESCENCE; ANXIETY; DEVELOPMENT; FEAR-POTENTIATED STARTLE; PUBERTY; SEX DIFFERENCES;

ACOUSTIC STIMULATION; ADOLESCENT; AFFECT; AGING; ANXIETY; CHILD; COHORT STUDIES; CROSS-SECTIONAL STUDIES; CUES; DEFENSE MECHANISMS; FEAR; FEMALE; GALVANIC SKIN RESPONSE; HUMANS; LARYNX; LONGITUDINAL STUDIES; MALE; PHOTIC STIMULATION; PHYSICAL STIMULATION; PROSPECTIVE STUDIES; PUBERTY; SEX CHARACTERISTICS; SEXUAL MATURATION; STARTLE REACTION;

EID: 84893977594     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2013.12.002     Document Type: Article

References (66)

1. Allen L.S., Gorski R.A. Sex difference in the bed nucleus of the stria terminalis of the human brain. Journal of Comparative Neurology 1990, 302(4):697-706.
2. Angold A., Costello E.J. Puberty and depression. Child and Adolescent Psychiatric Clinics of North America 2006, 15(4):919-937. ix.
3. Angold A., Costello E.J., Erkanli A., Worthman C.M. Pubertal changes in hormone levels and depression in girls. Psychological Medicine 1999, 29(5):1043-1053.
4. Armbruster D., Mueller A., Strobel A., Kirschbaum C., Lesch K.P., Brocke B. Influence of functional tryptophan hydroxylase 2 gene variation and sex on the startle response in children, young adults, and older adults. Biological Psychology 2010, 83(3):214-221.
5. Barker T.V., Reeb-Sutherland B.C., Fox N.A. Individual differences in fear potentiated startle in behaviorally inhibited children. Developmental Psychobiology 2013, 56(1):133-141.
6. Blanton R.E., Cooney R.E., Joormann J., Eugene F., Glover G.H., Gotlib I.H. Pubertal stage and brain anatomy in girls. Neuroscience 2012, 217:105-112.
7. Blumenthal T.D., Cuthbert B.N., Filion D.L., Hackley S., Lipp O.V., van Boxtel A. Committee report: Guidelines for human startle eyeblink electromyographic studies. Psychophysiology 2005, 42(1):1-15. 10.1111/j.1469-8986.2005.00271.x.
8. Borelli J.L., Sbarra D.A., Crowley M.J., Mayes L.C. Mood symptoms and emotional responsiveness to threat in school-aged children. Journal of Clinical Child and Adolescent Psychology 2011, 40(2):220-232.
9. Bradley M.M., Codispoti M., Sabatinelli D., Lang P.J. Emotion and motivation II: Sex differences in picture processing. Emotion 2001, 1(3):300-319.
10. Cameron J.L. Interrelationships between hormones, behavior, and affect during adolescence: Complex relationships exist between reproductive hormones, stress-related hormones, and the activity of neural systems that regulate behavioral affect. Comments on part III. Annals of the New York Academy of Sciences 2004, 1021:134-142.
11. Dahl R.E. Adolescent brain development: A period of vulnerabilities and opportunities. Keynote address. Annals of the New York Academy of Sciences 2004, 1021:1-22. 10.1196/annals.1308.001.
12. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: Role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35(1):105-135.
13. Essau C.A., Conradt J., Petermann F. Frequency of panic attacks and panic disorder in adolescents. Depression and Anxiety 1999, 9(1):19-26.
14. Fairchild G., Stobbe Y., van Goozen S.H., Calder A.J., Goodyer I.M. Facial expression recognition, fear conditioning, and startle modulation in female subjects with conduct disorder. Biological Psychiatry 2010, 68(3):272-279. 10.1016/j.biopsych.2010.02.019.
15. Fairchild G., Van Goozen S.H., Stollery S.J., Goodyer I.M. Fear conditioning and affective modulation of the startle reflex in male adolescents with early-onset or adolescence-onset conduct disorder and healthy control subjects. Biological Psychiatry 2008, 63(3):279-285. 10.1016/j.biopsych.2007.06.019.
16. Giedd J.N., Clasen L.S., Lenroot R., Greenstein D., Wallace G.L., Ordaz S., et al. Puberty-related influences on brain development. Molecular and Cellular Endocrinology 2006, 254-255:154-162.
17. Glenn C.R., Klein D.N., Lissek S., Britton J.C., Pine D.S., Hajcak G. The development of fear learning and generalization in 8-13 year-olds. Developmental Psychobiology 2012, 54(7):675-684.
18. Grillon C., Ameli R., Goddard A., Woods S.W., Davis M. Baseline and fear-potentiated startle in panic disorder patients. Biological Psychiatry 1994, 35(7):431-439.
19. Grillon C., Davis M. Fear-potentiated startle conditioning in humans: Explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology 1997, 34(4):451-458.
20. Grillon C. Models and mechanisms of anxiety: Evidence from startle studies. Psychopharmacology 2008, 199(3):421-437.
21. Grillon C., Baas J.P., Lissek S., Smith K., Milstein J. Anxious responses to predictable and unpredictable aversive events. Behavioral Neuroscience 2004, 118(5):916-924.
22. Grillon C., Dierker L., Merikangas K.R. Startle modulation in children at risk for anxiety disorders and/or alcoholism. Journal of the American Academy of Child and Adolescent Psychiatry 1997, 36(7):925-932.
23. Grillon C., Dierker L., Merikangas K.R. Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biological Psychiatry 1998, 44(10):990-997.
24. Grillon C., Merikangas K.R., Dierker L., Snidman N., Arriaga R.I., Kagan J., et al. Startle potentiation by threat of aversive stimuli and darkness in adolescents: A multi-site study. International Journal of Psychophysiology 1999, 32(1):63-73.
25. Hayward C., Killen J.D., Hammer L.D., Litt I.F., Wilson D.M., Simmonds B., et al. Pubertal stage and panic attack history in sixth- and seventh-grade girls. American Journal of Psychiatry 1992, 149(9):1239-1243.
26. Hayward C., Sanborn K. Puberty and the emergence of gender differences in psychopathology. Journal of Adolescent Health 2002, 30(4 Suppl.):49L 58.
27. Hillman C.H., Rosengren K.S., Smith D.P. Emotion and motivated behavior: Postural adjustments to affective picture viewing. Biological Psychology 2004, 66(1):51-62.
28. Hodes G.E., Shors T.J. Distinctive stress effects on learning during puberty. Hormones and Behavior 2005, 48(2):163-171.
29. Hyde J.S., Mezulis A.H., Abramson L.Y. The ABCs of depression: Integrating affective, biological, and cognitive models to explain the emergence of the gender difference in depression. Psychological Review 2008, 115(2):291-313.
30. Kim J.H., Richardson R. New findings on extinction of conditioned fear early in development: Theoretical and clinical implications. Biological Psychiatry 2010, 67(4):297-303. 10.1016/j.biopsych.2009.09.003.
31. Koch M. The neurobiology of startle. Progress in Neurobiology 1999, 59(2):107-128.
32. Lang P.J., Bradley M.M., Cuthbert B.N. Emotion, motivation, and anxiety: Brain mechanisms and psychophysiology. Biological Psychiatry 1998, 44(12):1248-1263.
33. Lang P.J., Davis M. Emotion, motivation, and the brain: Reflex foundations in animal and human research. Progress in Brain Research 2006, 156:3-29.
34. Lang P.J., Davis M., Ohman A. Fear and anxiety: Animal models and human cognitive psychophysiology. Journal of Affective Disorders 2000, 61(3):137-159.
35. LeResche L., Mancl L.A., Drangsholt M.T., Saunders K., Korff M.V. Relationship of pain and symptoms to pubertal development in adolescents. Pain 2005, 118(1-2):201-209.
36. Macaulay J.L., Kleinknecht R.A. Panic and panic attacks in adolescents. Journal of Anxiety Disorders 1989, 3(4):221-241.
37. McEwen B.S. Mood disorders and allostatic load. Biological Psychiatry 2003, 54(3):200-207.
38. McManis M.H., Bradley M.M., Berg W.K., Cuthbert B.N., Lang P.J. Emotional reactions in children: Verbal, physiological, and behavioral responses to affective pictures. Psychophysiology 2001, 38(2):222-231.
39. Morgan C.A., Grillon C., Southwick S.M., Davis M., Charney D.S. Fear-potentiated startle in posttraumatic stress disorder. Biological Psychiatry 1995, 38(6):378-385.
40. Morris N.M., Udry J.R. Validation of a self-administered instrument to assess stage of adolescent development. Journal of Youth and Adolescence 1980, 9(3):271-280.
41. Ordaz S., Luna B. Sex differences in physiological reactivity to acute psychosocial stress in adolescence. Psychoneuroendocrinology 2012, 37(8):1135-1157.
42. Palanza P. Animal models of anxiety and depression: How are females different?. Neuroscience and Biobehavioral Reviews 2001, 25(3):219-233.
43. Patton G.C., Hibbert M.E., Carlin J., Shao Q., Rosier M., Caust J., et al. Menarche and the onset of depression and anxiety in Victoria, Australia. Journal of Epidemiology and Community Health 1996, 50(6):661-666.
44. Patton G.C., Viner R. Pubertal transitions in health. Lancet 2007, 369(9567):1130-1139.
45. Pietropaolo S., Crusio W.E. Strain-dependent changes in acoustic startle response and its plasticity across adolescence in mice. Behavior Genetics 2009, 39(6):623-631.
46. Quevedo K., Benning S.D., Gunnar M.R., Dahl R.E. The onset of puberty: Effects on the psychophysiology of defensive and appetitive motivation. Development and Psychopathology 2009, 21(1):27-45.
47. Quevedo K., Smith T., Donzella B., Schunk E., Gunnar M. The startle response: Developmental effects and a paradigm for children and adults. Developmental Psychobiology 2010, 52(1):78-89. 10.1002/dev.20415.
48. Reardon L.E., Leen-Feldner E.W., Hayward C. A critical review of the empirical literature on the relation between anxiety and puberty. Clinical Psychology Review 2009, 29(1):1-23.
49. Reeb-Sutherland B.C., Helfinstein S.M., Degnan K.A., Perez-Edgar K., Henderson H.A., Lissek S., et al. Startle response in behaviorally inhibited adolescents with a lifetime occurrence of anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry 2009, 48(6):610-617.
50. Reed V., Wittchen H.U. DSM-IV panic attacks and panic disorder in a community sample of adolescents and young adults: How specific are panic attacks?. Journal of Psychiatric Research 1998, 32(6):335-345.
51. Rudy J.W. Contextual conditioning and auditory cue conditioning dissociate during development. Behavioral Neuroscience 1993, 107(5):887-891.
52. Schmitz A., Grillon C. Assessing fear and anxiety in humans using the threat of predictable and unpredictable aversive events (the NPU-threat test). Nature Protocols 2012, 7(3):527-532.
53. Schmitz A., Merikangas K., Swendsen H., Cui L., Heaton L., Grillon C. Measuring anxious responses to predictable and unpredictable threat in children and adolescents. Journal of Experimental Child Psychology 2011, 110(2):159-170.
54. Silberg J., Pickles A., Rutter M., Hewitt J., Simonoff E., Maes H., et al. The influence of genetic factors and life stress on depression among adolescent girls. Archives of General Psychiatry 1999, 56(3):225-232.
55. Silk J.S., Siegle G.J., Whalen D.J., Ostapenko L.J., Ladouceur C.D., Dahl R.E. Pubertal changes in emotional information processing: Pupillary, behavioral, and subjective evidence during emotional word identification. Development and Psychopathology 2009, 21(1):7-26.
56. Sisk C.L., Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology 2005, 26(3-4):163-174.
57. Somerville L.H., Jones R.M., Casey B.J. A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition 2010, 72(1):124-133. 10.1016/j.bandc.2009.07.003.
58. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 2000, 24(4):417-463.
59. Spear L.P. Heightened stress responsivity and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology 2009, 21(1):87-97.
60. Spielberger C.D., Gorssuch R.L., Lushene P.R., Vagg P.R., Jacobs G.A. Manual for the State-Trait Anxiety Inventory 1983, Consulting Psychologists Press, Inc., Palo Alto, CA.
61. Syngelaki E.M., Fairchild G., Moore S.C., Savage J.C., van Goozen S.H. Affective startle potentiation in juvenile offenders: The role of conduct problems and psychopathic traits. Soc Neurosci 2013, 8(2):112-121. 10.1080/17470919.2012.712549.
62. Toufexis D. Region- and sex-specific modulation of anxiety behaviours in the rat. Journal of Neuroendocrinology 2007, 19(6):461-473.
63. Walker D.L., Toufexis D.J., Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. European Journal of Pharmacology 2003, 463(1-3):199-216.
64. Warren R., Zgourides G. Panic attacks in high school students: Implications for prevention and intervention. Phobia Practice and Research Journal 1988, 1(2):97-113.
65. Waters A.M., Craske M.G., Bergman R.L., Naliboff B.D., Negoro H., Ornitz E.M. Developmental changes in startle reactivity in school-age children at risk for and with actual anxiety disorder. International Journal of Psychophysiology 2008, 70(3):158-164.
66. Waters A.M., Ornitz E.M. When the orbicularis oculi response to a startling stimulus is zero, the vertical EOG may reveal that a blink has occurred. Clinical Neurophysiology 2005, 116(9):2110-2120.