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New Research, Development

Development of the Functional Connectome Topology in Adolescence: Evidence from Topological Data Analysis

Zeus Gracia-Tabuenca, Juan Carlos Díaz-Patiño, Isaac Arelio-Ríos, Martha Beatriz Moreno-García, Fernando A. Barrios and Sarael Alcauter
eNeuro 30 January 2023, ENEURO.0296-21.2022; https://doi.org/10.1523/ENEURO.0296-21.2022
Zeus Gracia-Tabuenca
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
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Juan Carlos Díaz-Patiño
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
2Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada 22860, México
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Isaac Arelio-Ríos
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
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Martha Beatriz Moreno-García
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
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Fernando A. Barrios
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
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Sarael Alcauter
1Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro 76230, México
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Abstract

Adolescence is a crucial developmental period in terms of behavior and mental health. Therefore, understanding how the brain develops during this stage is a fundamental challenge for neuroscience. Recent studies have modeled the brain as a network or connectome, mainly applying measures from graph theory, showing a change in its functional organization, such as an increase in its segregation and integration. Topological Data Analysis (TDA) complements such modeling by extracting high-dimensional features across the whole range of connectivity values instead of exploring a fixed set of connections. This study inquires into the developmental trajectories of such properties using a longitudinal sample of typically developing human participants (N = 98; 53/45 female/male; 6.7–18.1 years), applying TDA to their functional connectomes. In addition, we explore the effect of puberty on individual developmental trajectories. Results showed that the adolescent brain has a more distributed topology structure compared with random networks but is more densely connected at the local level. Furthermore, developmental effects showed nonlinear trajectories for the topology of the whole brain and fronto-parietal networks, with an inflection point and increasing trajectories after puberty onset. These results add to the insights into the development of the functional organization of the adolescent brain.

Significance Statement

Topological Data Analysis (TDA) may be used to explore the topology of the brain along the whole range of connectivity values instead of selecting only a fixed set of connectivity thresholds. Here, we explored some properties of the topology of the brain’s functional connectome and how they develop in adolescence. We show that developmental trajectories are nonlinear and better adjusted by puberty status than chronological age, with an inflection point around the onset of puberty. In particular, the results show that the topology of the fronto-parietal network is the one that drives the functional connectome changes in the adolescent period.

  • adolescence
  • functional connectivity
  • persistence homology
  • puberty
  • resting state functional magnetic resonance imaging
  • topological data analysis

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Consejo Nacional de Ciencia y Tecnologia (CONACYT) Fellowship 330142 (to Z.G.-T.) for being a doctoral student of Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM), a Universidad Nacional Autónoma de México-Dirección General de Asuntos del Personal Académico (UNAM-DGAPA) postdoctoral fellowship, and UNAM-Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (UNAM-PAPIIT) Grants IN208622 and IN212219 (to S.A.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Development of the Functional Connectome Topology in Adolescence: Evidence from Topological Data Analysis
Zeus Gracia-Tabuenca, Juan Carlos Díaz-Patiño, Isaac Arelio-Ríos, Martha Beatriz Moreno-García, Fernando A. Barrios, Sarael Alcauter
eNeuro 30 January 2023, ENEURO.0296-21.2022; DOI: 10.1523/ENEURO.0296-21.2022

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Development of the Functional Connectome Topology in Adolescence: Evidence from Topological Data Analysis
Zeus Gracia-Tabuenca, Juan Carlos Díaz-Patiño, Isaac Arelio-Ríos, Martha Beatriz Moreno-García, Fernando A. Barrios, Sarael Alcauter
eNeuro 30 January 2023, ENEURO.0296-21.2022; DOI: 10.1523/ENEURO.0296-21.2022
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Keywords

  • adolescence
  • functional connectivity
  • persistence homology
  • puberty
  • resting state functional magnetic resonance imaging
  • topological data analysis

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