Skip to main content
SpringerLink
Log in

Effects of age, sex, and puberty on neural efficiency of cognitive and motor control in adolescents

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Critical changes in adolescence involve brain cognitive maturation of inhibitory control processes that are essential for a myriad of adult functions. Cognitive control advances into adulthood as there is more flexible integration of component processes, including inhibitory control of conflicting information, overwriting inappropriate response tendencies, and amplifying relevant responses for accurate execution. Using a modified Stroop task with fMRI, we investigated the effects of age, sex, and puberty on brain functional correlates of cognitive and motor control in 87 boys and 91 girls across the adolescent age range. Results revealed dissociable brain systems for cognitive and motor control processes, whereby adolescents flexibly adapted neural responses to control demands. Specifically, when response repetitions facilitated planning-based action selection, frontoparietal-insular regions associated with cognitive control operations were less activated, whereas cortical-pallidal-cerebellar motor regions associated with motor skill acquisition, were more activated. Attenuated middle cingulate cortex activation occurred with older adolescent age for both motor control and cognitive control with automaticity from repetition learning. Sexual dimorphism for control operations occurred in extrastriate cortices involved in visuo-attentional selection: While boys enhanced extrastriate selection processes for motor control, girls activated these regions more for cognitive control. These sex differences were attenuated with more advanced pubertal stage. Together, our findings show that brain cognitive and motor control processes are segregated, demand-specific, more efficient in older adolescents, and differ between sexes relative to pubertal development. Our findings advance our understanding of how distributed brain activity and the neurodevelopment of automaticity enhances cognitive and motor control ability in adolescence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adleman, N. E., Menon, V., Blasey, C. M., White, C. D., Warsofsky, I. S., Glover, G. H., & Reiss, A. L. (2002). A developmental fMRI study of the Stroop color-word task. Neuroimage., 16(1), 61–75.

    Article  PubMed  Google Scholar 

  • Akshoomoff, N., Newman, E., Thompson, W. K., McCabe, C., Bloss, C. S., Chang, L., Amaral, D. G., Casey, B. J., Ernst, T. M., Frazier, J. A., Gruen, J. R., Kaufmann, W. E., Kenet, T., Kennedy, D. N., Libiger, O., Mostofsky, S., Murray, S. S., Sowell, E. R., Schork, N., Dale, A. M., & Jernigan, T. L. (2014). The NIH toolbox cognition battery: Results from a large normative developmental sample (ping). Neuropsychology., 28, 1–10.

    Article  PubMed  Google Scholar 

  • Alarcón, G., Cservenka, A., Fair, D. A., & Nagel, B. J. (2014). Sex differences in the neural substrates of spatial working memory during adolescence are not mediated by endogenous testosterone. Brain Research, 1593, 40–54.

    Article  PubMed  CAS  Google Scholar 

  • Andrews-Hanna, J. R., Mackiewicz Seghete, K. L., Claus, E. D., Burgess, G. C., Ruzic, L., & Banich, M. T. (2011). Cognitive control in adolescence: Neural underpinnings and relation to self-report behaviors. PLoS One, 6(6), e21598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banich, M. T., Crowley, T. J., Thompson, L. L., Jacobson, B. L., Liu, X., Raymond, K. M., & Claus, E. D. (2007). Brain activation during the Stroop task in adolescents with severe substance and conduct problems: A pilot study. Drug and Alcohol Dependence, 90(2–3), 175–182.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barber, A. D., Caffo, B. S., Pekar, J. J., & Mostofsky, S. H. (2013). Effects of working memory demand on neural mechanisms of motor response selection and control. Journal of Cognitive Neuroscience, 25(8), 1235–1248.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beauchamp, M. H., Dagher, A., Aston, J. A., & Doyon, J. (2003). Dynamic functional changes associated with cognitive skill learning of an adapted version of the tower of London task. Neuroimage., 20(3), 1649–1660.

    Article  CAS  PubMed  Google Scholar 

  • Bench, C. J., Frith, C. D., Grasby, P. M., Friston, K. J., Paulesu, E., Frackowiak, R. S., & Dolan, R. J. (1993). Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia., 31(9), 907–922.

    Article  CAS  PubMed  Google Scholar 

  • Blakemore, S. J. (2008). The social brain in adolescence. Nature Reviews. Neuroscience, 9(4), 267–277 Review.

    Article  CAS  PubMed  Google Scholar 

  • Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., Li, W., Parrish, T. B., Gitelman, D. R., & Mesulam, M. M. (2003). Neural development of selective attention and response inhibition. Neuroimage., 20(2), 737–751.

    Article  PubMed  Google Scholar 

  • Breukelaar, I. A., Antees, C., Grieve, S. M., Foster, S. L., Gomes, L., Williams, L. M., & Korgaonkar, M. S. (2016). Cognitive control network anatomy correlates with neurocognitive behavior: A longitudinal study. Human Brain Mapping, 38(2), 631–643.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown, S. A., Brumback, T., Tomlinson, K., Cummins, K., Thompson, W. K., Nagel, B. J., De Bellis, M. D., Hooper, S. R., Clark, D. B., Chung, T., Hasler, B. P., Colrain, I. M., Baker, F. C., Prouty, D., Pfefferbaum, A., Sullivan, E. V., Pohl, K. M., Rohlfing, T., Nichols, B. N., Chu, W., & Tapert, S. F. (2015). The National Consortium on alcohol and NeuroDevelopment in adolescence (NCANDA): A multisite study of adolescent development and substance use. Journal of Studies on Alcohol and Drugs, 76(6), 895–908.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carter, C. S., Mintun, M., & Cohen, J. D. (1995). Interference and facilitation effects during selective attention: An H215O PET study of Stroop task performance. Neuroimage., 2(4), 264–272.

    Article  CAS  PubMed  Google Scholar 

  • Carter, C. S., Botvinick, M. M., & Cohen, J. D. (1999). The contribution of the anterior cingulate cortex to executive processes in cognition. Reviews in the Neurosciences, 10(1), 49–57.

    Article  CAS  PubMed  Google Scholar 

  • Casey, B. J., Tottenham, N., Liston, C., & Durston, S. (2005). Imaging the developing brain: What have we learned about cognitive development? Trends in Cognitive Sciences, 9(3), 104–110.

    Article  CAS  PubMed  Google Scholar 

  • Casey, B. J., Jones, R. M., & Hare, T. A. (2008). The adolescent brain. Annals of the New York Academy of Sciences, 1124, 111–126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chambers, C. D., Garavan, H., & Bellgrove, M. A. (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience and Biobehavioral Reviews, 33, 631–646.

    Article  PubMed  Google Scholar 

  • Chen, Z., Lei, X., Ding, C., Li, H., & Chen, A. (2013). The neural mechanisms of semantic and response conflicts: An fMRI study of practice-related effects in the Stroop task. Neuroimage., 66, 577–584.

    Article  PubMed  Google Scholar 

  • Christakou, A., Brammer, M., & Rubia, K. (2011). Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting. Neuroimage, 54, 1344–1354.

    Article  PubMed  Google Scholar 

  • Cohen, J. R., Gallen, C. L., Jacobs, E. G., Lee, T. G., & D’Esposito, M. (2014). Quantifying the reconfiguration of intrinsic networks during working memory. PLoS One, 9(9), e106636.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Comalli, P. E., Wapner, S., & Werner, H. (1962). Interference effects of Stroop color-word test in childhood, adulthood, and aging. The Journal of Genetic Psychology, 100, 47–53.

    Article  PubMed  Google Scholar 

  • Crone, E. A., & Dahl, R. E. (2012). Understanding adolescence as a period of social-affective engagement and goal flexibility. Nature Reviews. Neuroscience, 13(9), 636–650 Review.

    Article  CAS  PubMed  Google Scholar 

  • Cservenka, A., Stroup, M. L., Etkin, A., & Nagel, B. J. (2015). The effects of age, sex, and hormones on emotional conflict-related brain response during adolescence. Brain and Cognition, 99, 135–150.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dambacher, F., Sack, A. T., Lobbestael, J., Arntz, A., Brugman, S., & Schuhmann, T. (2015). Out of control: Evidence for anterior insula involvement in motor impulsivity and reactive aggression. Social Cognitive and Affective Neuroscience, 10(4), 508–516.

    Article  PubMed  Google Scholar 

  • Danielmeier, C., Zysset, S., Müsseler, J., & von Cramon, D. Y. (2004). Where action impairs visual encoding: An event-related fMRI study. Brain Research. Cognitive Brain Research, 21(1), 39–48.

    Article  PubMed  Google Scholar 

  • Egner, T., & Hirsch, J. (2005). The neural correlates and functional integration of cognitive control in a Stroop task. Neuroimage., 24(2), 539–547.

    Article  PubMed  Google Scholar 

  • Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences, 113(28), 7900–7905.

  • Erickson, K. I., Boot, W. R., Basak, C., Neider, M. B., Prakash, R. S., Voss, M. W., Graybiel, A. M., Simons, D. J., Fabiani, M., Gratton, G., & Kramer, A. F. (2010). Striatal volume predicts level of video game skill acquisition. Cerebral Cortex, 20(11), 2522–2530.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan, J., Flombaum, J. I., McCandliss, B. D., Thomas, K. M., & Posner, M. I. (2003). Cognitive and brain consequences of conflict. Neuroimage., 18(1), 42–57.

    Article  PubMed  Google Scholar 

  • Filbey, F. M., Schacht, J. P., Myers, U. S., Chavez, R. S., & Hutchison, K. E. (2009). Marijuana craving in the brain. Proceedings of the National Academy of Sciences of the United States of America, 106(31), 13016–13021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews. Neuroscience, 8, 700–711.

    Article  CAS  PubMed  Google Scholar 

  • Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102, 9673–9678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox, K. C., Spreng, R. N., Ellamil, M., Andrews-Hanna, J. R., & Christoff, K. (2015). The wandering brain: Meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes. Neuroimage, 111, 611–621.

    Article  PubMed  Google Scholar 

  • Geier, C. F., Terwilliger, R., Teslovich, T., Velanova, K., & Luna, B. (2010). Immaturities in reward processing and its influence on inhibitory control in adolescence. Cerebral Cortex, 20(7), 1613–1629.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Giedd, J. N., Raznahan, A., Mills, K. L., & Lenroot, R. K. (2012). Review: Magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biology of Sex Differences, 3(1), 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. F., 3rd, Herman, D. H., Clasen, L. S., Toga, A. W., Rapoport, J. L., & Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101(21), 8174–8179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gratton, G., Coles, M. G., & Donchin, E. (1992). Optimizing the use of information: Strategic control of activation of responses. Exp Psychol Gen., 121(4), 480–506.

    Article  CAS  Google Scholar 

  • Gur, R. C., Turetsky, B. I., Matsu, M., Yan, M., Bilker, W., Hughett, P., & Gur, R. E. (1999). Sex differences in brain gray and white matter in healthy young adults: Correlations with cognitive performance. The Journal of Neuroscience, 19, 4065–4072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herting, M. M., Gautam, P., Spielberg, J. M., Kan, E., Dahl, R. E., & Sowell, E. R. (2014). The role of testosterone and estradiol in brain volume changes across adolescence: A longitudinal structural MRI study. Human Brain Mapping, 35(11), 5633–5645.

  • Herting, M. M., Gautam, P., Spielberg, J. M., Dahl, R. E., & Sowell, E. R. (2015). A longitudinal study: Changes in cortical thickness and surface area during pubertal maturation. PLoS One, 10(3), e0119774.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang, B., Hillman, J., Biro, F. M., Ding, L., Dorn, L. D., & Susman, E. J. (2012). Correspondence between gonadal steroid hormone concentrations and secondary sexual characteristics assessed by clinicians, adolescents, and parents. Journal of Research on Adolescence, 22, 381–391.

    Article  PubMed  PubMed Central  Google Scholar 

  • Imamizu, H., & Kawato, M. (2009). Brain mechanisms for predictive control by switching internal models: Implications for higher-order cognitive functions. Psychological Research, 73(4), 527–544.

    Article  PubMed  Google Scholar 

  • Ito, M. (1993). Synaptic plasticity in the cerebellar cortex and its role in motor learning. The Canadian Journal of Neurological Sciences, 20(Supp 3), S70–S74 Review.

    PubMed  Google Scholar 

  • Juraska, J. M., & Willing, J. (2017). Pubertal onset as a critical transition for neural development and cognition. Brain Research, 1654(Pt B), 87–94 Review.

    Article  CAS  PubMed  Google Scholar 

  • Kelly, A. M., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X., & Milham, M. P. (2009). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cerebral Cortex, 19(3), 640–657.

    Article  PubMed  Google Scholar 

  • Kerns, J. G., Cohen, J. D., MacDonald, A. W., 3rd, Cho, R. Y., Stenger, V. A., & Carter, C. S. (2004a). Anterior cingulate conflict monitoring and adjustments in control. Science., 303(5660), 1023–1026.

    Article  CAS  PubMed  Google Scholar 

  • Kerns, J. G., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2004b). Prefrontal cortex guides context-appropriate responding during language production. Neuron., 43(2), 283–291.

    Article  CAS  PubMed  Google Scholar 

  • Koch, C., & Brown, J. M. (1994). Examining the time course of prime effects on Stroop processing. Perceptual and Motor Skills, 79(1 Pt 2), 675–687.

    Article  CAS  PubMed  Google Scholar 

  • Koolschijn, P. C., Peper, J. S., & Crone, E. A. (2014). The influence of sex steroids on structural brain maturation in adolescence. PLoS One, 9, e83929.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koziol, L. F., Budding, D. E., & Chidekel, D. (2012). From movement to thought: Executive function, embodied cognition, and the cerebellum. Cerebellum., 11(2), 505–525 Review.

    Article  PubMed  Google Scholar 

  • Ladouceur, C. D., Schlund, M. W., & Segreti, A. M. (2018). Positive reinforcement modulates fronto-limbic systems subserving emotional interference in adolescents. Behavioural Brain Research, 338, 109–117.

    Article  PubMed  Google Scholar 

  • Larrue, V., Celsis, P., Bès, A., & Marc-Vergnes, J. P. (1994). The functional anatomy of attention in humans: Cerebral blood flow changes induced by reading, naming, and the Stroop effect. Journal of Cerebral Blood Flow and Metabolism, 14(6), 958–962.

    Article  CAS  PubMed  Google Scholar 

  • Larson, M. J., Kaufman, D. A., & Perlstein, W. M. (2009). Neural time course of conflict adaptation effects on the Stroop task. Neuropsychologia., 47(3), 663–670.

    Article  PubMed  Google Scholar 

  • Leisman, G., Braun-Benjamin, O., & Melillo, R. (2014). Cognitive-motor interactions of the basal ganglia in development. Frontiers in Systems Neuroscience, 8, 16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, D., Zucker, N. L., Kragel, P. A., Covington, V. E., & LaBar, K. S. (2017). Adolescent development of insula-dependent interoceptive regulation. Developmental Science, 20(5). https://doi.org/10.1111/desc.12438.

  • Loeber, R., Burke, J., & Pardini, D. A. (2009). Perspectives on oppositional defiant disorder, conduct disorder, and psychopathic features. Journal of Child Psychology and Psychiatry, 50, 133–142.

    Article  PubMed  Google Scholar 

  • Luciana, M., Conklin, H. M., Hooper, C. J., & Yarger, R. S. (2005). The development of nonverbal working memory and executive control processes in adolescents. Child Development, 76(3), 697–712.

    Article  PubMed  Google Scholar 

  • Luna, B., Thulborn, K. R., Munoz, D. P., Merriam, E. P., Garver, K. E., Minshew, N. J., Keshavan, M. S., Genovese, C. R., Eddy, W. F., & Sweeney, J. A. (2001). Maturation of widely distributed brain function subserves cognitive development. Neuroimage., 13(5), 786–793.

    Article  CAS  PubMed  Google Scholar 

  • Luna, B., Marek, S., Larsen, B., Tervo-Clemmens, B., & Chahal, R. (2015). An integrative model of the maturation of cognitive control. Annual Review of Neuroscience, 38, 151–170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacDonald, A. W., 3rd, Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838.

    Article  CAS  PubMed  Google Scholar 

  • Marek, S., Hwang, K., Foran, W., Hallquist, M. N., & Luna, B. (2015). The contribution of network organization and integration to the development of cognitive control. PLoS Biology, 13(12), e1002328.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marusak, H. A., Etkin, A., & Thomason, M. E. (2015). Disrupted insula-based neural circuit organization and conflict interference in trauma-exposed youth. Neuroimage Clinics, 8, 516–525.

    Article  Google Scholar 

  • Mayr, U., Awh, E., & Laurey, P. (2003). Conflict adaptation effects in the absence of executive control. Nature Neuroscience, 6(5), 450–452.

    Article  CAS  PubMed  Google Scholar 

  • McCormick, E. M., & Telzer, E. H. (2018). Contributions of default mode network stability and deactivation to adolescent task engagement. Scientific Reports, 8(1), 18049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLeod, C. M. (1991). Half a century of research on the Stroop effect: An integrative review. Psychological Bulletin, 109, 163–203.

    Article  Google Scholar 

  • Melcher, T., & Gruber, O. (2006). Oddball and incongruity effects during Stroop task performance: A comparative fMRI study on selective attention. Brain Research, 1121(1), 136–149.

    Article  CAS  PubMed  Google Scholar 

  • Mishkin, M., Malamut, B., & Bachevalier, J. (1984). Memories and habits: Two neural systems. In G. Lynch, J. L. McGaugh, & N. M. Weinberger (Eds.), Neurobiology of learning and memory (pp. 65–77). New York: Guilford.

    Google Scholar 

  • Müller-Oehring, E. M., Kwon, D., Nagel, B. J., Sullivan, E. V., Chu, W., Rohlfing, T., Prouty, D., Nichols, B. N., Poline, J. B., Tapert, S. F., Brown, S. A., Cummins, K., Brumback, T., Colrain, I. M., Baker, F. C., De Bellis, M. D., Voyvodic, J. T., Clark, D. B., Pfefferbaum, A., & Pohl, K. M. (2017). Influences of age, sex, and moderate alcohol drinking on the intrinsic functional architecture of adolescent brains. Cerebral Cortex, 28(3), 1049–1063. https://doi.org/10.1093/cercor/bhx014.

  • Nguyen, T. V., McCracken, J., Ducharme, S., Botteron, K. N., Mahabir, M., Johnson, W., Israel, M., Evans, A. C., Karama, S., & Brain Development Cooperative Group. (2013). Testosterone-related cortical maturation across childhood and adolescence. Cerebral Cortex, 23(6), 1424–1432.

    Article  PubMed  Google Scholar 

  • Nguyen, T. V., Gower, P., Albaugh, M. D., Botteron, K. N., Hudziak, J. J., Fonov, V. S., Collins, L., Ducharme, S., & McCracken, J. T. (2016). The developmental relationship between DHEA and visual attention is mediated by structural plasticity of cortico-amygdalar networks. Psychoneuroendocrinology., 70, 122–133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen, T. V., Lew, J., Albaugh, M. D., Botteron, K. N., Hudziak, J. J., Fonov, V. S., Collins, D. L., Ducharme, S., & McCracken, J. T. (2017). Sex-specific associations of testosterone with prefrontal-hippocampal development and executive function. Psychoneuroendocrinology., 76, 206–217.

    Article  CAS  PubMed  Google Scholar 

  • Op de Macks, Z. A., Bunge, S. A., Bell, O. N., Wilbrecht, L., Kriegsfeld, L. J., Kayser, A. S., & Dahl, R. E. (2016). Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry. Psychoneuroendocrinology., 74, 77–91.

    Article  CAS  Google Scholar 

  • Pardo, J. V., Pardo, P. J., Janer, K. W., & Raichle, M. E. (1990). The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proceedings of the National Academy of Sciences of the United States of America, 87(1), 256–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen, A. C., 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.

    Article  CAS  PubMed  Google Scholar 

  • Peterson, B. S., Skudlarski, P., Gatenby, J. C., Zhang, H., Anderson, A. W., & Gore, J. C. (1999). An fMRI study of Stroop word-color interference: Evidence for cingulate subregions subserving multiple distributed attentional systems. Biological Psychiatry, 45(10), 1237–1258.

    Article  CAS  PubMed  Google Scholar 

  • Pfefferbaum, A., Rohlfing, T., Pohl, K. M., Lane, B., Chu, W., Kwon, D., Nolan Nichols, B., Brown, S. A., Tapert, S. F., Cummins, K., Thompson, W. K., Brumback, T., Meloy, M. J., Jernigan, T. L., Dale, A., Colrain, I. M., Baker, F. C., Prouty, D., De Bellis, M. D., Voyvodic, J. T., Clark, D. B., Luna, B., Chung, T., Nagel, B. J., & Sullivan, E. V. (2016). Adolescent development of cortical and White matter structure in the NCANDA sample: Role of sex, ethnicity, puberty, and alcohol drinking. Cerebral Cortex, 26(10), 4101–4121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfefferbaum, A., Kwon, D., Brumback, T., Thompson, W. K., Cummins, K., Tapert, S. F., Brown, S. A., Colrain, I. M., Baker, F. C., Prouty, D., De Bellis, M. D., Clark, D. B., Nagel, B. J., Chu, W., Park, S. H., Pohl, K. M., & Sullivan, E. V. (2018). Altered brain developmental trajectories in adolescents after initiating drinking. The American Journal of Psychiatry, 175(4), 370–380.

    Article  PubMed  Google Scholar 

  • Piekarski, D. J., Boivin, J. R., & Wilbrecht, L. (2017). Ovarian hormones organize the maturation of inhibitory neurotransmission in the frontal cortex at puberty onset in female mice. Current Biology, 27(12), 1735–1745.

    Article  CAS  PubMed  Google Scholar 

  • Poldrack, R. A. (2002). Neural systems for perceptual skill learning. Behavioral and Cognitive Neuroscience Reviews, 1(1), 76–83 Review.

    Article  PubMed  Google Scholar 

  • Poldrack, R. A., Sabb, F. W., Foerde, K., Tom, S. M., Asarnow, R. F., Bookheimer, S. Y., & Knowlton, B. J. (2005). The neural correlates of motor skill automaticity. The Journal of Neuroscience, 25(22), 5356–5364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Power, J. D., Fair, D. A., Schlaggar, B. L., & Petersen, S. E. (2010). The development of human functional brain networks. Neuron, 67(5), 735–748 Review.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purmann, S., & Pollmann, S. (2015). Adaptation to recent conflict in the classical color-word Stroop-task mainly involves facilitation of processing of task-relevant information. Frontiers in Human Neuroscience, 9, 88.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raichle, M. E. (2011). The restless brain. Brain Connectivity, 1(1), 3–12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rainer, G., Lee, H., & Logothetis, N. K. (2004). The effect of learning on the function of monkey extrastriate visual cortex. PLoS Biology, 2(2), E44.

    Article  PubMed  PubMed Central  Google Scholar 

  • Randerath, J., Valyear, K. F., Philip, B. A., & Frey, S. H. (2017). Contributions of the parietal cortex to increased efficiency of planning-based action selection. Neuropsychologia., 105, 135–143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raznahan, A., Shaw, P. W., Lerch, J. P., Clasen, L. S., Greenstein, D., Berman, R., Pipitone, J., Chakravarty, M. M., & Giedd, J. N. (2014). Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proceedings of the National Academy of Sciences of the United States of America, 111(4), 1592–1597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28(11), 1163–1177.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rubia, K., Lim, L., Ecker, C., Halari, R., Giampietro, V., Simmons, A., Brammer, M., & Smith, A. (2013). Effects of age and gender on neural networks of motor response inhibition: From adolescence to mid-adulthood. Neuroimage, 83, 690–703.

    Article  PubMed  Google Scholar 

  • Sali, A. W., Courtney, S. M., & Yantis, S. (2016). Spontaneous fluctuations in the flexible control of covert attention. The Journal of Neuroscience, 36(2), 445–454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saling, L. L., & Phillips, J. G. (2007). Automatic behaviour: Efficient not mindless. Brain Research Bulletin, 73(1–3), 1–20.

    Article  CAS  PubMed  Google Scholar 

  • Salo, R., Henik, A., & Robertson, L. C. (2001). Interpreting Stroop interference: An analysis of differences between task versions. Neuropsychology., 15(4), 462–471.

    Article  CAS  PubMed  Google Scholar 

  • Satterthwaite, T. D., Wolf, D. H., Erus, G., Ruparel, K., Elliott, M. A., Gennatas, E. D., Hopson, R., Jackson, C., Prabhakaran, K., Bilker, W. B., Calkins, M. E., Loughead, J., Smith, A., Roalf, D. R., Hakonarson, H., Verma, R., Davatzikos, C., Gur, R. C., & Gur, R. E. (2013). Functional maturation of the executive system during adolescence. The Journal of Neuroscience, 33(41), 16249–16261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satterthwaite, T. D., Vandekar, S., Wolf, D. H., Ruparel, K., Roalf, D. R., Jackson, C., Elliott, M. A., Bilker, W. B., Calkins, M. E., Prabhakaran, K., Davatzikos, C., Hakonarson, H., Gur, R. E., & Gur, R. C. (2014). Sex differences in the effect of puberty on hippocampal morphology. Journal of the American Academy of Child and Adolescent Psychiatry, 53(3), 341–350.e1.

    Article  PubMed  Google Scholar 

  • Satterthwaite, T. D., Wolf, D. H., Roalf, D. R., Ruparel, K., Erus, G., Vandekar, S., Gennatas, E. D., Elliott, M. A., Smith, A., Hakonarson, H., Verma, R., Davatzikos, C., Gur, R. E., & Gur, R. C. (2015). Linked sex differences in cognition and functional connectivity in youth. Cerebral Cortex, 25(9), 2383–2394.

    Article  PubMed  Google Scholar 

  • Savic, I., Frisen, L., Manzouri, A., Nordenstrom, A., & Lindén Hirschberg, A. (2017). Role of testosterone and Y chromosome genes for the masculinization of the human brain. Human Brain Mapping, 38(4), 1801–1814.

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheinost, D., Finn, E. S., Tokoglu, F., Shen, X., Papademetris, X., Hampson, M., & Constable, R. T. (2015). Sex differences in normal age trajectories of functional brain networks. Human Brain Mapping, 36(4), 1524–1535.

    Article  PubMed  Google Scholar 

  • Schmidt, J. R., & Weissman, D. H. (2016). Congruency sequence effects and previous response times: Conflict adaptation or temporal learning? Psychological Research, 80(4), 590–607.

    Article  PubMed  Google Scholar 

  • Schramm-Sapyta, N. L., Walker, Q. D., Caster, J. M., Levin, E. D., & Kuhn, C. M. (2009). Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology, 206(1), 1–21 Review.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeter, M. L., Zysset, S., Wahl, M., & von Cramon, D. Y. (2004). Prefrontal activation due to Stroop interference increases during development--an event-related fNIRS study. Neuroimage., 23(4), 1317–1325.

    Article  PubMed  Google Scholar 

  • Schulte, T., Müller-Oehring, E. M., Chanraud, S., Rosenbloom, M. J., Pfefferbaum, A., & Sullivan, E. V. (2011). Age-related reorganization of functional networks for successful conflict resolution: A combined functional and structural MRI study. Neurobiology of Aging, 32(11), 2075–2090.

    Article  PubMed  Google Scholar 

  • Schulte, T., Müller-Oehring, E. M., Sullivan, E. V., & Pfefferbaum, A. (2012). Synchrony of corticostriatal-midbrain activation enables normal inhibitory control and conflict processing in recovering alcoholic men. Biological Psychiatry, 71(3), 269–278.

    Article  PubMed  Google Scholar 

  • 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. The Journal of Neuroscience, 27(9), 2349–2356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selmeczy, D., Fandakova, Y., Grimm, K. J., Bunge, S. A., & Ghetti, S. (2018). Longitudinal trajectories of hippocampal and prefrontal contributions to episodic retrieval: Effects of age and puberty. Developmental Cognitive Neuroscience, S1878-9293(18), 30132–30134.

    Google Scholar 

  • Shen, X. (2005). Sex differences in perceptual processing: Performance on the color-kanji stroop task of visual stimuli. The International Journal of Neuroscience, 115, 1631–1641.

    Article  PubMed  Google Scholar 

  • Simmonds, D. J., Hallquist, M. N., & Luna, B. (2017). Protracted development of executive and mnemonic brain systems underlying working memory in adolescence: A longitudinal fMRI study. Neuroimage, 157, 695–704.

    Article  PubMed  Google Scholar 

  • Spielberg, J. M., Galarce, E. M., Ladouceur, C. D., McMakin, D. L., Olino, T. M., Forbes, E. E., Silk, J. S., Ryan, N. D., & Dahl, R. E. (2015). Adolescent development of inhibition as a function of SES and gender: Converging evidence from behavior and fMRI. Human Brain Mapping, 36(8), 3194–3203.

    Article  PubMed  PubMed Central  Google Scholar 

  • Squeglia, L. M., McKenna, B. S., Jacobus, J., Castro, N., Sorg, S. F., & Tapert, S. F. (2013). BOLD response to working memory not related to cortical thickness during early adolescence. Brain Research, 1537, 59–68.

    Article  CAS  PubMed  Google Scholar 

  • Stevens, M. C. (2016). The contributions of resting state and task-based functional connectivity studies to our understanding of adolescent brain network maturation. Neuroscience and Biobehavioral Reviews, 70, 13–32.

    Article  PubMed  Google Scholar 

  • Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 12, 643–662.

    Article  Google Scholar 

  • Supekar, K., & Menon, V. (2012). Developmental maturation of dynamic causal control signals in higher-order cognition: A neurocognitive network model. PLoS Computational Biology, 8(2), e1002374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamm, L., Menon, V., & Reiss, A. L. (2002). Maturation of brain function associated with response inhibition. Journal of the American Academy of Child and Adolescent Psychiatry, 41(10), 1231–1238.

    Article  PubMed  Google Scholar 

  • 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(9), 2731–2745.

    Article  PubMed  Google Scholar 

  • Tomasi, D., Ernst, T., Caparelli, E. C., & Chang, L. (2006). Common deactivation patterns during working memory and visual attention tasks: An intra-subject fMRI study at 4 tesla. Human Brain Mapping, 27(8), 694–705.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tremel, J. J., Laurent, P. A., Wolk, D. A., Wheeler, M. E., & Fiez, J. A. (2016). Neural signatures of experience-based improvements in deterministic decision-making. Behavioural Brain Research, 315, 51–65.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyborowska, A., Volman, I., Smeekens, S., Toni, I., & Roelofs, K. (2016). Testosterone during puberty shifts emotional control from Pulvinar to anterior prefrontal cortex. The Journal of Neuroscience, 36(23), 6156–6164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullsperger, M., Bylsma, L. M., & Botvinick, M. M. (2005). The conflict adaptation effect: it's not just priming. Cognitive, Affective, & Behavioral Neuroscience, 5(4), 467–472.

    Article  Google Scholar 

  • van Duijvenvoorde, A. C. (2016). What motivates adolescents? Neural responses to rewards and their influence on adolescents’ risk taking, learning, and cognitive control. Neuroscience and Biobehavioral Reviews, 70, 135–147.

    Article  PubMed  Google Scholar 

  • Veroude, K., Jolles, J., Croiset, G., & Krabbendam, L. (2013). Changes in neural mechanisms of cognitive control during the transition from late adolescence to young adulthood. Developmental Cognitive Neuroscience, 5, 63–70.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogel, A. C., Power, J. D., Petersen, S. E., & Schlaggar, B. L. (2010). Development of the Brain’s functional network architecture. Neuropsychology Review, 20(4), 362–375.

    Article  PubMed  Google Scholar 

  • White, H. R., Marmorstein, N. R., Crews, F. T., Bates, M. E., Mun, E. Y., & Loeber, R. (2011). Associations between heavy drinking and changes in impulsive behavior among adolescent boys. Alcoholism, Clinical and Experimental Research, 35(2), 295–303.

    Article  PubMed  Google Scholar 

  • Wierenga, L. M., Bos, M. G. N., Schreuders, E., Vd Kamp, F., Peper, J. S., Tamnes, C. K., & Crone, E. A. (2018). Unraveling age, puberty and testosterone effects on subcortical brain development across adolescence. Psychoneuroendocrinology., 91, 105–114.

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson, G. S., & Robertson, G. J. (2006). Wide range achievement test (WRAT4). Psychological assessment resources. In Lutz.

    Google Scholar 

  • Wu, T., & Hallett, M. (2005). The influence of normal human ageing on automatic movements. The Journal of Physiology, 562(Pt 2), 605–615.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, T., Cao, M., Niu, H., Zuo, X. N., Evans, A., He, Y., Dong, Q., & Shu, N. (2015). Age-related changes in the topological organization of the white matter structural connectome across the human lifespan. Human Brain Mapping, 36(10), 3777–3792.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the U.S. National Institute on Alcohol Abuse and Alcoholism with co-funding from the National Institute on Drug Abuse, the National Institute of Mental Health, the National Institute of Health Office of the Director, the National Institute of Child Health and Human Development, and the Office of the Director, National Institutes of Health [NCANDA grant numbers: AA021696 (IMC + FCB), AA021695 (SAB + SFT), AA021692 (SFT), AA021697 (AP + KMP)]. Additional funding was provided by NIAAA grant number AA010723 (EVS).

Author information

Authors and Affiliations

  1. Center for Health Sciences, Neuroscience Program, Biosciences Division, SRI International, Menlo Park, CA, 94025-3493, USA

    Tilman Schulte, Jui-Yang Hong, Adolf Pfefferbaum, Fiona C. Baker, Weiwei Chu, Devin Prouty, Dongjin Kwon, Ian M. Colrain & Eva M. Müller-Oehring

  2. Pacific Graduate School of Clinical Psychology, Palo Alto University, Palo Alto, CA, USA

    Tilman Schulte

  3. Department of Psychiatry & Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA

    Edith V. Sullivan, Adolf Pfefferbaum, Dongjin Kwon & Eva M. Müller-Oehring

  4. Department of Psychiatry, University of California, San Diego, La Jolla, CA, USA

    Mary J. Meloy, Ty Brumback & Susan F. Tapert

Authors
  1. Tilman Schulte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jui-Yang Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edith V. Sullivan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adolf Pfefferbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fiona C. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weiwei Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Devin Prouty
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dongjin Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mary J. Meloy
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ty Brumback
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Susan F. Tapert
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ian M. Colrain
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Eva M. Müller-Oehring
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tilman Schulte.

Ethics declarations

Conflict of interest

None of the authors have conflicts of interest with the reported data or their interpretation.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 393 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schulte, T., Hong, JY., Sullivan, E.V. et al. Effects of age, sex, and puberty on neural efficiency of cognitive and motor control in adolescents. Brain Imaging and Behavior 14, 1089–1107 (2020). https://doi.org/10.1007/s11682-019-00075-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-019-00075-x

Keywords

Search

Navigation