Frontoparietal structural connectivity in childhood predicts development of functional connectivity and reasoning ability: A large-scale longitudinal investigation

Journal of Neuroscience

Volumn 37, Issue 35, 2017, Pages 8549-8558

  Wendelken, Carter ^a,b   Ferrer, Emilio ^c   Ghetti, Simona ^c   Bailey, Stephen K ^d   Cutting, Laurie ^d   Bunge, Silvia A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VICARIOUS AI   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

FMRI; Functional connectivity; Longitudinal; Reasoning; Structural connectivity

Indexed keywords

ARTICLE; CHILD; COGNITION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FOLLOW UP; FRONTOPARIETAL CORTEX; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; PARIETAL LOBE; PRIORITY JOURNAL; TRACTOGRAPHY; WHITE MATTER; ADOLESCENT; AGING; ANATOMY AND HISTOLOGY; BRAIN MAPPING; DECISION MAKING; FRONTAL LOBE; NERVE CELL NETWORK; NERVE TRACT; PHYSIOLOGY; PROGNOSIS; YOUNG ADULT;

ADOLESCENT; AGING; BRAIN MAPPING; CHILD; COGNITION; DECISION MAKING; FEMALE; FRONTAL LOBE; HUMANS; LONGITUDINAL STUDIES; MALE; NERVE NET; NEURAL PATHWAYS; PARIETAL LOBE; PROGNOSIS; WHITE MATTER; YOUNG ADULT;

EID: 85028684778     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3726-16.2017     Document Type: Article

References (40)

1. Asato MR, Terwilliger R, Woo J, Luna B (2010) White matter development in adolescence: a DTI study. Cereb Cortex 20:2122–2131. CrossRef Medline
2. Barber AD, Caffo BS, Pekar JJ, Mostofsky SH (2013) Developmental changes in within and between-network connectivity between late childhood and adulthood. Neuropsychologia 51:156–167. CrossRef Medline
3. Bazargani N, Hillebrandt H, Christoff K, Dumontheil I (2014) Developmental changes in effective connectivity associated with relational reasoning. Hum Brain Mapp 35:3262–3276. CrossRef Medline
4. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088. CrossRef Medline
5. Cocchi L, Halford GS, Zalesky A, Harding IH, Ramm BJ, Cutmore T, Shum DH, Mattingley JB (2014) Complexity in relational processing predicts changes in functional brain network dynamics. Cereb Cortex 24:2283– 2296. CrossRef Medline
6. Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83:238– 251. CrossRef Medline
7. Ernst M, Torrisi S, Balderston N, Grillon C, Hale EA (2015) fMRI functional connectivity applied to adolescent neurodevelopment. Annu Rev Clin Psychol 11:361–377. CrossRef Medline
8. Fair DA, Schlaggar BL, Cohen AL, Miezin FM, Dosenbach NU, Wenger KK, Fox MD, Snyder AZ, Raichle ME, Petersen SE (2007) A method for using blocked and event-related fMRI data to study “resting state” functional connectivity. Neuroimage 35:396–405. CrossRef Medline
9. Ferrer E, O’Hare E, Bunge S (2009) Fluid reasoning and the developing brain. Front Neurosci 3:46–51. CrossRef Medline
10. Ferrer E, Whitaker KJ, Steele JS, Green CT, Wendelken C, Bunge SA (2013) White matter maturation supports the development of reasoning ability through its influence on processing speed. Dev Sci 16:941–951. CrossRef Medline
11. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78. CrossRef Medline
12. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A 106:2035–2040. CrossRef Medline
13. Horn A, Ostwald D, Reisert M, Blankenburg F (2014) The structural-functional connectome and the default mode network of the human brain. Neuroimage 102:142–151. CrossRef Medline
14. Jung RE, Haier RJ (2007) The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30: 135–154; discussion 154–187. CrossRef Medline
15. Khalsa S, Mayhew SD, Chechlacz M, Bagary M, Bagshaw AP (2014) The structural and functional connectivity of the posterior cingulate cortex: comparison between deterministic and probabilistic tractography for the investigation of structure-function relationships. Neuroimage 102:118– 127. CrossRef Medline
16. Krawczyk DC (2012) The cognition and neuroscience of relational reasoning. Brain Res 1428:13–23. CrossRef Medline
17. Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352. CrossRef Medline
18. McArdle JJ, Ferrer-Caja E, Hamagami F, Woodcock RW (2002) Comparative longitudinal structural analyses of the growth and decline of multiple intellectual abilities over the life span. Dev Psychol 38:115–142. CrossRef Medline
19. Peters BD, Ikuta T, DeRosse P, John M, Burdick KE, Gruner P, Prendergast DM, Szeszko PR, Malhotra AK (2014) age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biol Psychiatry 75:248–256. CrossRef Medline
20. Pinheiro J, Bates D, DebRoy S, Sarkar D; R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1–109.
21. Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL, Petersen SE (2011) Functional network organization of the human brain. Neuron 72:665–678. CrossRef Medline
22. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154. CrossRef Medline
23. Prado J, Chadha A, Booth JR (2011) The brain network for deductive reasoning: a quantitative meta-analysis of 28 neuroimaging studies. J Cogn Neurosci 23:3483–3497. CrossRef Medline
24. R Core Team (2013) R: A language and environment for statistical computing. Available from: http://www.R-project.org/. Accessed: January 1, 2016.
25. Sastre M 3rd, Wendelken C, Lee JK, Bunge SA, Ghetti S (2016) age and performance-related differences in hippocampal contributions to episodic memory retrieval. Dev Cogn Neurosci 19:42–50. CrossRef Medline
26. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356. CrossRef Medline
27. Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J (2006) Intellectual ability and cortical development in children and adolescents. Nature 440:676–679. CrossRef Medline
28. Shokri-Kojori E, Motes MA, Rypma B, Krawczyk DC (2012) The network architecture of cortical processing in visuo-spatial reasoning. Sci Rep 2:411. CrossRef Medline
29. Siegel JS, Mitra A, Laumann TO, Seitzman BA, Raichle M, Corbetta M, and Snyder A (2016) Data quality influences observed links between functional connectivity and behavior. Cereb Cortex. In press.
30. Skudlarski P, Jagannathan K, Calhoun VD, Hampson M, Skudlarska BA, Pearlson G (2008) Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43:554– 561. CrossRef Medline
31. Smit DJ, Boersma M, Schnack HG, Micheloyannis S, Boomsma DI, Hulshoff Pol HE, Stam CJ, de Geus EJ (2012) The brain matures with stronger functional connectivity and decreased randomness of its network. PLoS One 7:e36896. CrossRef Medline
32. Tamnes CK, Østby Y, Walhovd KB, Westlye LT, Due-Tønnessen P, Fjell AM (2010) Intellectual abilities and white matter microstructure in development: a diffusion tensor imaging study. Hum Brain Mapp 31:1609–1625. CrossRef Medline
33. Vendetti MS, Bunge SA (2014) Evolutionary and developmental changes in the lateral frontoparietal network: a little goes a long way for higher-level cognition. Neuron 84:906–917. CrossRef Medline
34. Wechsler D (1974) Manual for the Wechsler Intelligence Scale for Children–Revised. New York: The Psychological Corporation.
35. Wendelken C, Bunge SA (2010) Transitive inference: distinct contributions of rostrolateral prefrontal cortex and the hippocampus. J Cogn Neurosci 22:837–847. CrossRef Medline
36. Wendelken C, O’Hare ED, Whitaker KJ, Ferrer E, Bunge SA (2011) Increased functional selectivity over development in rostrolateral prefrontal cortex. J Neurosci 31:17260–17268. CrossRef Medline
37. Wendelken C, Chung D, and Bunge SA (2012) Rostrolateral prefrontal cortex: domain-general or domain-sensitive? Hum Brain Mapp 33:1952– 1963. CrossRef Medline
38. Wendelken C, Ferrer E, Whitaker KJ, Bunge SA (2016) Fronto-parietal network reconfiguration supports the development of reasoning ability. Cereb Cortex 26:2178–2190. CrossRef Medline
39. Woodcock RW, McGrew KS, Mather N (2001) Woodcock Johnson III Tests of Achievement. Rolling Meadows, IL: Riverside.
40. Wright SB, Matlen BJ, Baym CL, Ferrer E, Bunge SA (2007) Neural correlates of fluid reasoning in children and adults. Front Hum Neurosci 1:8. CrossRef Medline