Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T16:22:39.388Z Has data issue: false hasContentIssue false
  • English
  • Français

The onset of puberty: Effects on the psychophysiology of defensive and appetitive motivation

Published online by Cambridge University Press:  15 January 2009

Karina M. Quevedo ,
Stephen D. Benning ,
Megan R. Gunnar  and
Ronald E. Dahl
Karina M. Quevedo*
Affiliation:
University of Minnesota
Stephen D. Benning
Affiliation:
Vanderbilt University
Megan R. Gunnar
Affiliation:
University of Minnesota
Ronald E. Dahl
Affiliation:
University of Pittsburgh School of Medicine
*
Address correspondence and reprint requests to: Karina M. Quevedo, Institute of Child Development, 51 East River Road, Minneapolis, MN 55455-0345; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined puberty-specific effects on affect-related behavior and on the psychophysiology of defensive and appetitive motivation while controlling for age. Adolescents (N = 94, ages = 12 and 13 years) viewed 75 pictures (International Affective Picture System: pleasant, neutral, and aversive) while listening to auditory probes. Startle response and postauricular (PA) reflex were collected as measures of defensive and appetitive motivation, respectively. Pubertal status and measures of anxiety/stress reaction and sensation/thrill seeking were obtained. Mid-/late pubertal adolescents showed enhanced startle amplitude across all picture valences. A Puberty × Valence interaction revealed that mid-/late pubertal adolescents showed appetitive potentiation of the PA, whereas pre-/early pubertal adolescents showed no modulation of the PA reflex. Mid-/late pubertal adolescents also scored significantly higher on measures of sensation/thrill seeking than did their pre-/early pubertal peers and puberty moderated the association between psychophysiology and behavioral measures, suggesting that it plays a role in reorganizing defensive and appetitive motivational systems.

Type
Special Section Articles
Information
Development and Psychopathology , Volume 21 , Issue 1 , January 2009 , pp. 27 - 45
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, G. R., & Berzonsky, M. D. (Eds.). (2003). Blackwell handbook of adolescence. Malden, MA: Blackwell.Google Scholar
Andersen, S. L., Thompson, A. T., Rutstein, M., Hostetter, J. C., & Teicher, M. H. (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse, 37, 167–169.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Avenevoli, S., Merikangas, K. R., Stolar, M., & Grillon, C. (2003). Pubertal development, startle modulation, and changes in affective expression. Paper presented at the Society for Research in Child Development Biennial MeetingTampa, FL.Google Scholar
Barb, C. R., Hausman, G. J., & Czaja, K. (2005). Leptin: A metabolic signal affecting central regulation of reproduction in the pig. Domestic Animal Endocrinology, 29, 186–192.CrossRefGoogle Scholar
Benning, S. (2006). Embedding the postauricular reflex in a psychophysiological nomological network of emotion: Modulation by pictures, sounds, and dysphoria. Minneapolis, MN: University of Minnesota.Google Scholar
Benning, S., Patrick, C., & Lang, A. R. (2004). Emotional modulation of the post-auricular reflex. Psychophysiology, 41, 426–432.CrossRefGoogle ScholarPubMed
Benning, S. D., Patrick, C. J., & Iacono, W. G. (2005). Psychopathy, startle blink modulation, and electrodermal reactivity in twin men. Psychophysiology, 42, 753–762.CrossRefGoogle ScholarPubMed
Berzin, F., & Fortinguerra, C. R. (1993). Emg study of the anterior, superior and posterior auricular muscles in man. Annals of Anatomy, 175, 195–197.CrossRefGoogle ScholarPubMed
Blumenthal, T. D., Cuthbert, B. N., Filion, D. L., Hackley, S., Lipp, O. V., & van Boxtel, A. (2005). Committee report: Guidelines for human startle eyeblink electromyographic studies. Psychophysiology, 42, 1–15.CrossRefGoogle ScholarPubMed
Bochenek, W., & Bochenek, Z. (1976). Postauricular (12 msec latency) responses to acoustic stimuli in patients with peripheral, facial nerve palsy. Acta Oto-Laryngologica, 81, 264–269.CrossRefGoogle ScholarPubMed
Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: The self-assessment manikin and the semantic differential. Journal of Behavior Therapy and Experimental Psychiatry, 25, 49–59.CrossRefGoogle ScholarPubMed
Brooks-Gunn, J., Warren, M. P., Rosso, J., & Gargiulo, J. (1987). Validity of self-report measures of girls' pubertal status. Child Development, 58, 829–841.CrossRefGoogle ScholarPubMed
Carskadon, M. A., Acebo, C., & Jenni, O. G. (2004). Regulation of adolescent sleep: Implications for behavior. Annals of the New York Academy of Sciences, 1021, 276–291.CrossRefGoogle ScholarPubMed
Carskadon, M. A., Harvey, K., Duke, P., Anders, T. F., Litt, I. F., & Dement, W. C. (1980). Pubertal changes in daytime sleepiness. Sleep, 2, 453–460.Google ScholarPubMed
Cicchetti, D., Rogosch, F. A., & Toth, S. L. (1994). A developmental psychopathology perspective on depression in children and adolescents. In Reinolds, W. M. & Johnston, H. F. (Eds.), Handbook of depression in children and adolescents. New York: Plenum Press.Google Scholar
Conklin, H. M., Luciana, M., Hooper, C. J., & Yarger, R. S. (2007). Working memory performance in typically developing children and adolescents: Behavioral evidence of protracted frontal lobe development. Developmental Neuropsychology, 31, 103–128.CrossRefGoogle ScholarPubMed
Dahl, R. E. (2004). Regulation of sleep and arousal: Comments on part vii. In Adolescent brain development: Vulnerabilities and opportunities (pp. 292–293). New York: New York Academy of Sciences.Google ScholarPubMed
Dahl, R. E., & Spear, L. P. (2004). Adolescent brain development: Vulnerabilities and opportunities (Vol. 1021). New York: New York Academy of Sciences.Google ScholarPubMed
Daitzman, R. J., Zuckerman, M., Sammelwitz, P., & Ganjam, V. (1978). Sensation seeking and gonadal hormones. Journal of Biosocial Science, 10, 401–408.CrossRefGoogle ScholarPubMed
Davis, M. (1988). The potentiated startle response as a measure of conditioned fear and its relevance to the neurobiology of anxiety. In Simon, P. & Soubrie, P. (Eds.), Selected models of anxiety, depression and psychosis animal models of psychiatric disorders (Vol. 1, pp. 61–89). Basel: Karger.Google Scholar
Davis, M., Falls, W. A., Campeau, S., & Kim, M. (1993). Fear-potentiated startle: A neural and pharmacological analysis. Behavioural Brain Research, 58, 175–198.CrossRefGoogle ScholarPubMed
Davis, M., Gendelman, D. S., Tischler, M. D., & Gendelman, P. M. (1982). A primary acoustic startle circuit: Lesion and stimulation studies. Journal of Neuroscience, 2, 791–805.CrossRefGoogle ScholarPubMed
Douek, E., & Clarke, G. P. (1976). A single average crossed acoustic response. The Journal of Laryngology and Otology, 90, 1027–1032.CrossRefGoogle ScholarPubMed
Eccles, J. S. (1999). The development of children ages 6 to 14. The Future of Children, 9, 30–44.CrossRefGoogle ScholarPubMed
Ernst, M., Pine, D. S., & Hardin, M. (2006). Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine, 36, 299–312.CrossRefGoogle ScholarPubMed
Fendt, M., Koch, M., & Schnitzler, H.-U. (1994). Amygdaloid noradrenaline is involved in the sensitization of the acoustic startle response in rats. Pharmacology, Biochemistry, and Behavior, 48, 307–314.CrossRefGoogle ScholarPubMed
Fleming, A. S., & Corter, M. (1995). Psychobiology of maternal behavior in nonhuman mammals. In Bornstein, M. (Ed.), Handbook of parenting (pp. 59–86). Hillside, NJ: Erlbaum.Google Scholar
Galvan, A. (2006). Neural substrates and development of reward-related behavior. Cornell, NY: Cornell University, Weill Medical College.Google Scholar
Ge, X., Kim, I. J., Brody, G. H., Conger, R. D., Simons, R. L., Gibbons, F. X., et al. (2003). It's about timing and change: Pubertal transition effects on symptoms of major depression among african american youths. Developmental Psychology, 39, 430–439.CrossRefGoogle ScholarPubMed
Genazzani, A. R., Bernardi, F., Monteleone, P., Luisi, S., & Luisi, M. (2000). Neuropeptides, neurotransmitters, neurosteroids, and the onset of puberty. Annals of the New York Academy of Sciences, 900, 1–9.CrossRefGoogle ScholarPubMed
Gore, A. C., & Terasawa, E. (1991). A role for norepinephrine in the control of puberty in the female rhesus monkey, Macaca mulatta. Endocrinology, 129, 3009–3017.Google ScholarPubMed
Granger, D. A., Shirtcliff, E. A., Zahn-Waxler, C., Usher, B., Klimes-Dougan, B., & Hastings, P. (2003). Salivary testosterone diurnal variation and psychopathology in adolescent males and females: Individual differences and developmental effects. Development and Psychopathology, 15, 431–449.CrossRefGoogle ScholarPubMed
Greist, J. H. (1995). The diagnosis of social phobia. The Journal of Clinical Psychiatry, 56 (Suppl. 5), 5–12.Google Scholar
Grillon, C., Ameli, R., Foot, M., & Davis, M. (1993). Fear-potentiated startle: Relationship to the level of state/trait anxiety in healthy subjects. Biological Psychiatry, 33, 566–574.CrossRefGoogle Scholar
Grillon, C., & Baas, J. M. P. (2002). Comments on the use of the startle reflex in psychopharmacological challenges: Impact of baseline startle on measurement of fear-potentiated startle. Psychopharmacology (Berlin), 164, 236–238.Google ScholarPubMed
Grillon, C., Dierker, L., & Merikangas, K. R. (1998). Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biological Psychiatry, 44, 990–997.CrossRefGoogle ScholarPubMed
Grunbaum, J. A., Kann, L., Kinchen, S. A., Williams, B., Ross, J. G., Lowry, R., et al. (2002). Youth risk behavior surveillance. MMWR Surveillance Summaries, 51, 1–62.Google ScholarPubMed
Hess, U., Sabourin, G., & Kleck, R. E. (2007). Postauricular and eyeblink startle responses to facial expressions. Psychophysiology, 44, 431–435.CrossRefGoogle ScholarPubMed
Huerta, R., & Brizuela-Gamino, O. L. (2002). Interaction of pubertal status, mood and self-esteem in adolescent girls. Journal of Reproductive Medicine, 47, 217–225.Google ScholarPubMed
Klorman, R., Cicchetti, D., Thatcher, J. E., & Ison, J. R. (2003). Acoustic startle in maltreated children. Journal of Abnormal Child Psychology, 31, 359–370.CrossRefGoogle ScholarPubMed
Kumari, V., Cotter, P., Corr, P. J., Gray, J. A., & Checkley, S. A. (1996). Effect of clonidine on the human acoustic startle reflex. Psychopharmacology (Berlin), 123, 353–360.CrossRefGoogle ScholarPubMed
Lang, P. J. (1980). Behavioral treatment and bio-behavioral assessment: Computer applications. In Sidowski, J. B., Johnson, J. H., & Williams, T. A. (Eds.), Technology in mental health care delivery systems (pp. 119–137). New York: Ablex.Google Scholar
Lang, P. J. (1995). The emotion probe. Studies of motivation and attention. The American Psychologist, 50, 372–385.CrossRefGoogle ScholarPubMed
Lang, P. J., & Bradley, M. M. (Eds.). (1999). International affective picture system (IAPS): Instruction manual and affective ratings (Tech. Rep. No. A-4). Gainesville, FL: University of Florida, Center for Research in Psychophysiology.Google Scholar
Larson, R., & Richards, M. H. (1991). Daily companionship in late childhood and early adolescence: Changing developmental contexts. Child Development, 62, 284–300.CrossRefGoogle ScholarPubMed
Laviola, G., Adriani, W., Terranova, M. L., & Gerra, G. (1999). Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neuroscience and Biobehavioral Reviews, 23, 993–1010.CrossRefGoogle ScholarPubMed
Laviola, G., Macri, S., Morley-Fletcher, S., & Adriani, W. (2003). Risk-taking behavior in adolescent mice: Psychobiological determinants and early epigenetic influence. Neuroscience and Biobehavioral Reviews, 27, 19–31.CrossRefGoogle ScholarPubMed
Lee, Y., Lopez, D. E., Meloni, E. G., & Davis, M. (1996). A primary acoustic startle pathway: Obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. Journal of Neuroscience, 16, 3775–3789.Google Scholar
Little, R. J. A. (1988). A test of missing completely at random for multivariate data with missing values. Journal of the American Statistical Association, 83, 1198–1202.CrossRefGoogle Scholar
Lissek, S., & Powers, A. S. (2003). Sensation seeking and startle modulation by physically threatening images. Biological Psychology, 63, 179–197.CrossRefGoogle ScholarPubMed
Martin, C. A., Kelly, T. H., Rayens, M. K., Brogli, B. R., Brenzel, A., Smith, J., et al. (2002). Sensation seeking, puberty and nicotine, alcohol, and marijuana use in adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 1495–1502.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1994). Corticosteroids and hippocampal plasticity. Annals of the New York Academy of Sciences, 746, 134–144.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Alves, S. E. (1999). Estrogen actions in the central nervous system. Endocrine Reviews, 20, 279–307.Google Scholar
McManis, M. H., Bradley, M. M., Berg, W., Cuthbert, B. N., & Lang, P. J. (2001). Emotional reactions in children: Verbal, physiological, and behavioral responses to affective pictures. Psychophysiology, 38, 222–231.Google Scholar
Morgan, C. A. 3rd, Grillon, C., Southwick, S. M., Nagy, L. M., Davis, M., Krystal, J. H., et al. (1995). Yohimbine facilitated acoustic startle in combat veterans with post-traumatic stress disorder. Psychopharmacology (Berlin), 117, 466–471.CrossRefGoogle ScholarPubMed
Morgan, C. A. 3rd, Southwick, S. M., Grillon, C., Davis, M., Krystal, J. H., & Charney, D. S. (1993). Yohimbine-facilitated acoustic startle reflex in humans. Psychopharmacology (Berlin), 110, 342–346.CrossRefGoogle ScholarPubMed
Nelson, E. E., Leibenluft, E., McClure, E., & Pine, D. S. (2005). The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163–174.Google Scholar
Patrick, C. J., Curtin, J. J., & Tellegen, A. (2002). Development and validation of a brief form of the multidimensional personality questionnaire. Psychological Assessment, 14, 150–163.Google Scholar
Patton, G. C., & Viner, R. (2007). Pubertal transitions in health. Lancet, 369, 1130–1139.CrossRefGoogle ScholarPubMed
Patuzzi, R. B., & O'Beirne, G. A. (1999). A correlation method for detecting the sound-evoked post-auricular muscle response (PAMR). Hearing Research, 138, 147–162.CrossRefGoogle ScholarPubMed
Petersen, A., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17, 117–133.CrossRefGoogle ScholarPubMed
Pine, D. S., Cohen, P., Gurley, D., Brook, J., & Ma, Y. (1998). The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Archives of General Psychiatry, 55, 56–64.CrossRefGoogle ScholarPubMed
Reynolds, C. R., & Kamphaus, R. W. (1998). Behavior Assessment System for Children; Behavioral assessment of children. Circle Pines, MN: American Guidance Service.Google Scholar
Romeo, R. D. (2001). The pubertal maturation of male sexual behavior: The role of steroid hormones, their receptors, and pheromones. East Lansing, MI: Michigan State University.Google Scholar
Rosen, J. B., & Schulkin, J. (1998). From normal fear to pathological anxiety. Psychological Review, 105, 325–350.Google Scholar
Roth, M. (1999). The differentiation of self-consciousness in adolescence. Zeitschrift fur Differentielle und Diagnostische Psychologie, 20, 116–125.CrossRefGoogle Scholar
Russo, M. F. (1991). A sensation seeking scale for children: Further refinement and psychometric development. Athens, GA: University of Georgia.Google Scholar
Russo, M. F., Stokes, G. S., Benjamin, B. L., Christ, M. A. G., McBurnett, K., Loeber, R., et al. (1993). A sensation seeking scale for children: Further refinement and psychometric development. Journal of Psychopathology and Behavioral Assessment, 15, 69–86.CrossRefGoogle Scholar
Sevy, S., Hassoun, Y., Bechara, A., Yechiam, E., Napolitano, B., Burdick, K., et al. (2006). Emotion-based decision-making in healthy subjects: Short-term effects of reducing dopamine levels. Psychopharmacology, 188, 228–235.Google Scholar
Shirtcliff, E. A., Dorshorst, J. J., Nguyen, J., & Pollak, S. D. (2006). Pubertal maturation and age influence adolescent's perception of the impact of recent negative life events. Paper presented at the 2006 Biennial Meeting of the Society for Child Development.Google Scholar
Shirtcliff, E. A., Heiligenstein, M., Hoornstra, L., Squires, K., & Pollak, S. D. (2007). Raging hormones? Stages of pubertal development largely capture underlying hormonal processes in early adolescence. Paper presented at the Society for Research in Child Development 2007 Biennial Meeting.Google Scholar
Sollers, J. J., & Hackley, S. A. (1997). Effects of foreperiod duration on reflexive and voluntary responses to intense noise bursts. Psychophysiology, 34, 518–526.CrossRefGoogle ScholarPubMed
Spear, L. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463.Google Scholar
Steinberg, L. (1989). Pubertal maturationa and parent-adolescent distance: An evolutionary perspective. In Adams, G. R., Montemayor, R., & Gullota, T. P. (Eds.), Advances in adolescent behavior and development (pp. 71–97). Newbury Park, CA: Sage.Google Scholar
Steinberg, L., Dahl, R., Keating, D., Kupfer, D. J., Masten, A. S., & Pine, D. S. (2006). The study of developmental psychopathology in adolescence: Integrating affective neuroscience with the study of context. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 2. Developmental neuroscience (2nd ed., pp. 710–741). Hoboken, NJ: Wiley.Google Scholar
Teinturier, C. (2002). Neuroendocrine mechanisms of puberty onset. Gynecologie, Obstetrique & Fertilite, 30, 809–813.CrossRefGoogle ScholarPubMed
Tellegen, A. (1985). Structures of mood and personality and their relevance to assessing anxiety, with an emphasis on self-report. In Tuma, A. H. & Maser, J. (Eds.), Anxiety and the anxiety disorders. Hillsdale, NJ: Erlbaum.Google Scholar
Twitchell, G. R., Hanna, G. L., Cook, E. H., Fitzgerald, H. E., & Zucker, R. A. (2000). Serotonergic function, behavioral disinhibition, and negative affect in children of alcoholics: The moderating effects of puberty. Alcoholism, Clinical and Experimental Research, 24, 972–979.CrossRefGoogle ScholarPubMed
Volkow, N. D., Fowler, J. S., & Wang, G. J. (2004). The addicted human brain viewed in the light of imaging studies: Brain circuits and treatment strategies. Neuropharmacology, 47 (Suppl. 1), 3–13.CrossRefGoogle Scholar
Weise, M., Eisenhofer, G., & Merke, D. P. (2002). Pubertal and gender-related changes in the sympathoadrenal system in healthy children. Clinical Endocrinology and Metabolism, 87, 5038–5043.CrossRefGoogle ScholarPubMed
Wu, M. F., Suzuki, S. S., & Siegel, J. M. (1988). Anatomical distribution and response patterns of reticular neurons active in relation to acoustic startle. Brain Research, 457, 399–406.Google Scholar
Yoshie, N., & Okudaira, T. (1969). Myogenic evoked potential responses to clicks in man. Acta Oto-Laryngologica, 252, 89–103.CrossRefGoogle ScholarPubMed
Young, L. J., Murphy Young, A. Z., & Hammock, E. A. (2005). Anatomy and neurochemistry of the pair bond. Journal of Comparative Neurology, 493, 51–57.Google Scholar