Skip to main content Accessibility help
×
Home

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

  • Karina M. Quevedo (a1), Stephen D. Benning (a2), Megan R. Gunnar (a1) and Ronald E. Dahl (a3)

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.

Copyright

Corresponding author

Address correspondence and reprint requests to: Karina M. Quevedo, Institute of Child Development, 51 East River Road, Minneapolis, MN 55455-0345; E-mail: queve001@umn.edu.

References

Hide All
Adams, G. R., & Berzonsky, M. D. (Eds.). (2003). Blackwell handbook of adolescence. Malden, MA: Blackwell.
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, 167169.
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.
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, 186192.
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.
Benning, S., Patrick, C., & Lang, A. R. (2004). Emotional modulation of the post-auricular reflex. Psychophysiology, 41, 426432.
Benning, S. D., Patrick, C. J., & Iacono, W. G. (2005). Psychopathy, startle blink modulation, and electrodermal reactivity in twin men. Psychophysiology, 42, 753762.
Berzin, F., & Fortinguerra, C. R. (1993). Emg study of the anterior, superior and posterior auricular muscles in man. Annals of Anatomy, 175, 195197.
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, 115.
Bochenek, W., & Bochenek, Z. (1976). Postauricular (12 msec latency) responses to acoustic stimuli in patients with peripheral, facial nerve palsy. Acta Oto-Laryngologica, 81, 264269.
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, 4959.
Brooks-Gunn, J., Warren, M. P., Rosso, J., & Gargiulo, J. (1987). Validity of self-report measures of girls' pubertal status. Child Development, 58, 829841.
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, 276291.
Carskadon, M. A., Harvey, K., Duke, P., Anders, T. F., Litt, I. F., & Dement, W. C. (1980). Pubertal changes in daytime sleepiness. Sleep, 2, 453460.
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.
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, 103128.
Dahl, R. E. (2004). Regulation of sleep and arousal: Comments on part vii. In Adolescent brain development: Vulnerabilities and opportunities (pp. 292293). New York: New York Academy of Sciences.
Dahl, R. E., & Spear, L. P. (2004). Adolescent brain development: Vulnerabilities and opportunities (Vol. 1021). New York: New York Academy of Sciences.
Daitzman, R. J., Zuckerman, M., Sammelwitz, P., & Ganjam, V. (1978). Sensation seeking and gonadal hormones. Journal of Biosocial Science, 10, 401408.
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. 6189). Basel: Karger.
Davis, M., Falls, W. A., Campeau, S., & Kim, M. (1993). Fear-potentiated startle: A neural and pharmacological analysis. Behavioural Brain Research, 58, 175198.
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, 791805.
Douek, E., & Clarke, G. P. (1976). A single average crossed acoustic response. The Journal of Laryngology and Otology, 90, 10271032.
Eccles, J. S. (1999). The development of children ages 6 to 14. The Future of Children, 9, 3044.
Ernst, M., Pine, D. S., & Hardin, M. (2006). Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine, 36, 299312.
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, 307314.
Fleming, A. S., & Corter, M. (1995). Psychobiology of maternal behavior in nonhuman mammals. In Bornstein, M. (Ed.), Handbook of parenting (pp. 5986). Hillside, NJ: Erlbaum.
Galvan, A. (2006). Neural substrates and development of reward-related behavior. Cornell, NY: Cornell University, Weill Medical College.
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, 430439.
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, 19.
Gore, A. C., & Terasawa, E. (1991). A role for norepinephrine in the control of puberty in the female rhesus monkey, Macaca mulatta. Endocrinology, 129, 30093017.
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, 431449.
Greist, J. H. (1995). The diagnosis of social phobia. The Journal of Clinical Psychiatry, 56 (Suppl. 5), 512.
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, 566574.
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, 236238.
Grillon, C., Dierker, L., & Merikangas, K. R. (1998). Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biological Psychiatry, 44, 990997.
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, 162.
Hess, U., Sabourin, G., & Kleck, R. E. (2007). Postauricular and eyeblink startle responses to facial expressions. Psychophysiology, 44, 431435.
Huerta, R., & Brizuela-Gamino, O. L. (2002). Interaction of pubertal status, mood and self-esteem in adolescent girls. Journal of Reproductive Medicine, 47, 217225.
Klorman, R., Cicchetti, D., Thatcher, J. E., & Ison, J. R. (2003). Acoustic startle in maltreated children. Journal of Abnormal Child Psychology, 31, 359370.
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, 353360.
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. 119137). New York: Ablex.
Lang, P. J. (1995). The emotion probe. Studies of motivation and attention. The American Psychologist, 50, 372385.
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.
Larson, R., & Richards, M. H. (1991). Daily companionship in late childhood and early adolescence: Changing developmental contexts. Child Development, 62, 284300.
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, 9931010.
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, 1931.
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, 37753789.
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, 11981202.
Lissek, S., & Powers, A. S. (2003). Sensation seeking and startle modulation by physically threatening images. Biological Psychology, 63, 179197.
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, 14951502.
McEwen, B. S. (1994). Corticosteroids and hippocampal plasticity. Annals of the New York Academy of Sciences, 746, 134144.
McEwen, B. S., & Alves, S. E. (1999). Estrogen actions in the central nervous system. Endocrine Reviews, 20, 279307.
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, 222231.
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, 466471.
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, 342346.
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, 163174.
Patrick, C. J., Curtin, J. J., & Tellegen, A. (2002). Development and validation of a brief form of the multidimensional personality questionnaire. Psychological Assessment, 14, 150163.
Patton, G. C., & Viner, R. (2007). Pubertal transitions in health. Lancet, 369, 11301139.
Patuzzi, R. B., & O'Beirne, G. A. (1999). A correlation method for detecting the sound-evoked post-auricular muscle response (PAMR). Hearing Research, 138, 147162.
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, 117133.
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, 5664.
Reynolds, C. R., & Kamphaus, R. W. (1998). Behavior Assessment System for Children; Behavioral assessment of children. Circle Pines, MN: American Guidance Service.
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.
Rosen, J. B., & Schulkin, J. (1998). From normal fear to pathological anxiety. Psychological Review, 105, 325350.
Roth, M. (1999). The differentiation of self-consciousness in adolescence. Zeitschrift fur Differentielle und Diagnostische Psychologie, 20, 116125.
Russo, M. F. (1991). A sensation seeking scale for children: Further refinement and psychometric development. Athens, GA: University of Georgia.
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, 6986.
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, 228235.
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.
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.
Sollers, J. J., & Hackley, S. A. (1997). Effects of foreperiod duration on reflexive and voluntary responses to intense noise bursts. Psychophysiology, 34, 518526.
Spear, L. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417463.
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. 7197). Newbury Park, CA: Sage.
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. 710741). Hoboken, NJ: Wiley.
Teinturier, C. (2002). Neuroendocrine mechanisms of puberty onset. Gynecologie, Obstetrique & Fertilite, 30, 809813.
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.
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, 972979.
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), 313.
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, 50385043.
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, 399406.
Yoshie, N., & Okudaira, T. (1969). Myogenic evoked potential responses to clicks in man. Acta Oto-Laryngologica, 252, 89103.
Young, L. J., Murphy Young, A. Z., & Hammock, E. A. (2005). Anatomy and neurochemistry of the pair bond. Journal of Comparative Neurology, 493, 5157.

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed