Adolescence is associated with genomically patterned consolidation of the hubs of the human brain connectome

Whitaker, Kirstie; Vértes, Petra E.; Romero-García, Rafael; Váša, František; Moutoussis, Michael; Prabhu, Gita; Weiskopf, Nikolaus; Callaghan, Martina F.; Wagstyl, Konrad; Rittman, Timothy; Tait, Roger; Ooi, Cinly; Suckling, John; Inkster, Becky; Fonagy, Peter; Dolan, Raymond J.; Jones, Peter B.; Goodyer, Ian; Bullmore, Edward T.

doi:10.1073/pnas.1601745113

Cited by 481 publications

(595 citation statements)

References 58 publications

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“…Alternatively it is possible that cortical thinning is a relatively subtle change and requires more statistical power to detect. Moreover, during development, including adolescence, there are widespread changes in cortical tissue composition and connectivity47 including in paralimbic networks 48. As such, the distributed network of changes seen in adults but not in children might depend on these late‐emerging structural maturations.…”

Section: Discussionmentioning

confidence: 99%

Multimodal computational neocortical anatomy in pediatric hippocampal sclerosis

Adler

Blackwood

Northam

et al. 2018

Ann Clin Transl Neurol

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ObjectiveIn contrast to adult cohorts, neocortical changes in epileptic children with hippocampal damage are not well characterized. Here, we mapped multimodal neocortical markers of epilepsy‐related structural compromise in a pediatric cohort of temporal lobe epilepsy and explored how they relate to clinical factors.MethodsWe measured cortical thickness, gray–white matter intensity contrast and intracortical FLAIR intensity in 22 patients with hippocampal sclerosis (HS) and 30 controls. Surface‐based linear models assessed between‐group differences in morphological and MR signal intensity markers. Structural integrity of the hippocampus was measured by quantifying atrophy and FLAIR patterns. Linear models were used to evaluate the relationships between hippocampal and neocortical MRI markers and clinical factors.ResultsIn the hippocampus, patients demonstrated ipsilateral atrophy and bilateral FLAIR hyperintensity. In the neocortex, patients showed FLAIR signal hyperintensities and gray–white matter boundary blurring in the ipsilesional mesial and lateral temporal neocortex. In contrast, cortical thinning was minimal and restricted to a small area of the ipsilesional temporal pole. Furthermore, patients with a history of febrile convulsions demonstrated more pronounced FLAIR hyperintensity in the ipsilesional temporal neocortex.InterpretationPediatric HS patients do not yet demonstrate the widespread cortical thinning present in adult cohorts, which may reflect consequences of a protracted disease process. However, pronounced temporal neocortical FLAIR hyperintensity and blurring of the gray–white matter boundary are already detectable, suggesting that alterations in MR signal intensities may reflect a different underlying pathophysiology that is detectable earlier in the disease and more pervasive in patients with a history of febrile convulsions.

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Section: Discussionmentioning

confidence: 99%

Multimodal computational neocortical anatomy in pediatric hippocampal sclerosis

Adler

Blackwood

Northam

et al. 2018

Ann Clin Transl Neurol

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“…For example, MRI measures that are sensitive to intracortical myelin have revealed a pattern of high myelin content in primary sensorimotor regions, which systematically decreases toward transmodal areas in parietal, temporal, and particularly prefrontal cortex [3,[25][26][27][28] (Figure 1A). A similar spatial distribution has been described for MRI-based measures of cortical thickness [12] and myelinated thickness [29].…”

Section: Glossarymentioning

confidence: 99%

Large-Scale Gradients in Human Cortical Organization

Huntenburg

Bazin

Margulies

2018

Trends in Cognitive Sciences

751

738

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Recent advances in mapping cortical areas in the human brain provide a basis for investigating the significance of their spatial arrangement. Here we describe a dominant gradient in cortical features that spans between sensorimotor and transmodal areas. We propose that this gradient constitutes a core organizing axis of the human cerebral cortex, and describe an intrinsic coordinate system on its basis. Studying the cortex with respect to these intrinsic dimensions can inform our understanding of how the spectrum of cortical function emerges from structural constraints. The Significance of Cortical LocationFor more than a century, neuroscientists have studied the cerebral cortex by delineating individual cortical areas (see Glossary) and mapping their function [1]. This agenda has substantially advanced in recent years, as automated parcellation methods improve and data sets of unprecedented size and quality become available [2][3][4]. Nevertheless, our understanding of how the complex structure of the cerebral cortex emerges and gives rise to its elaborate functions remains fragmentary. To complement the description of individual cortical areas, we propose an inquiry into the significance of their spatial arrangement, asking the basic question: Why are cortical areas located where they are?Early formulations of this question date to theories from classical neuroanatomy [1,[5][6][7]. They state that the spatial layout of cortical areas is not arbitrary, but a consequence of developmental mechanisms, shaped through evolutionary selection. The location of an area among its neighbors thus provides insight into its microstructural characteristics [6], its connections to other parts of the brain [7], and eventually its position in global processing hierarchies [8]. Consider, for example, the well-researched visual system of the macaque monkey [9,10]. Along the visual hierarchy, low-level visual features are increasingly abstracted and integrated with information from other systems. Traditionally, areas are ordered based on their degree of microstructural differentiation, and the classification of their connections as feedforward or feedback [11]. The framework we advocate emphasizes that an area's position in the visual processing hierarchy -and thus many of its microstructural and connectional features -is strongly related to its distance from the primary visual area [12,13].More generally, we propose that the spatial arrangement of areas along a global gradient between sensorimotor and transmodal regions is a key feature of human cortical organization. A gradient is an axis of variance in cortical features, along which areas fall in a spatially continuous order. Areas that resemble each other with respect to the feature of interest occupy similar positions along the gradient. As we will point out, there is a strong relationship between the similarity of two areas -that is, their relative position along the gradient -and their relative position along the cortical surface. This important role of cortical location pro...

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“…The cerebral cortex gets thinner between the ages of 14 and 24, with the greatest amount of change in the association cortex (the regions used for complex thought and reasoning) (15). Indeed, we are born with more neurons than we'll ever have during our life, and one of the most important developmental processes -the synaptic refinement, known as "pruning", eliminates some of the connections to ensure our brain is working more efficiently (15).…”

Section: Puberty and Neurodevelopmentmentioning

confidence: 99%

“…The other regions of the brain are more similar to their adult structure and their development is slowing down by the age of 14. Considering the importance of synapses being pruned away, it makes sense to keep as many synapses as needed for a longer time, until it is known which connections will be most efficient for optimal reasoning in the complex world around us (15). Using MRI to measure cortical thickness and intracortical myelination in 14-24 year old volunteers, it was found and replicated that associative cortical areas were thicker and less myelinated than primary cortical areas at the age of 14; however, the associative cortex had faster rates of shrinkage and myelination over the course of adolescence (15).…”

Section: Puberty and Neurodevelopmentmentioning

confidence: 99%

“…Considering the importance of synapses being pruned away, it makes sense to keep as many synapses as needed for a longer time, until it is known which connections will be most efficient for optimal reasoning in the complex world around us (15). Using MRI to measure cortical thickness and intracortical myelination in 14-24 year old volunteers, it was found and replicated that associative cortical areas were thicker and less myelinated than primary cortical areas at the age of 14; however, the associative cortex had faster rates of shrinkage and myelination over the course of adolescence (15). Adolescent cortical myelination and shrinkage were coupled, and specifically associated with the enriched expression of the synaptic, oligodendroglial and schizophrenia-related genes (15).…”

Section: Puberty and Neurodevelopmentmentioning

confidence: 99%

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The adolescent brain: Changes and challenges of development

Pejović-Milovančević¹,

Krgovic²,

Mitkovic-Voncina³

2017

Med podmladak

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Adolescence is a period between childhood and adulthood, characterized by specific physical and psychological development. It is a transitional developmental period, rather than a single snapshot in time. Traditional neurobiological and cognitive explanations of adolescent development of behavior have failed to account for the changes in behavior observed during adolescence. Magnetic resonance imaging studies have discovered that myelinogenesis continues from childhood to adulthood in the brain's region-specific neurocircuitry, which remains structurally and functionally vulnerable to impulsive habits. The maturation of the adolescent brain is influenced by heredity, environment, and sex, and they play a crucial role in myelination. Furthermore, one of the measures extracted out of MRI studies is also the thickness of cerebral cortex, a part that harbors synapses. It is the complexity of these synapses that allows humans to generate and understand complex thoughts and feelings in the real world, including the ability to solve analogies. And it is the complexity of those connections, remaining under construction during adolescence, that may be responsible for immature and impulsive behavior and neurobehavioral excitement during the adolescent life. 9 SAŽETAK Adolescencija je period fizičkog i psihološkog razvoja, koji se odvija između detinjstva i perioda odraslog života. To je više prelazni razvojni period nego što je izolovan trenutak u vremenu. Tradicionalna neurobiološka i kognitivna objašnjenja razvoja adolescenta nisu uspela da obrazlože promene u ponašanju koje se primećuju tokom adolescencije. Naučne studije su otkrile da se mijelogeneza nastavlja u specifičnim neuronskim mrežama mozga od detinjstva do zrelosti. Sazrevanje adolescentnog mozga je pod uticajem nasleđa, okruženja i pola, koji igraju presudnu ulogu u mijelinizaciji. Složenost razvoja sinapsi omogućava ljudima stvaranje i razumevanje kompleksnih misli i oseća-nja, uključujući i sposobnost rešavanja analogija u realnom svetu. I sama kompleksnost ovih veza, koje nastavljaju razvoj tokom adolescencije, može da bude odgovorna kako za nezrelo i impulsivno ponašanje, tako i za neurobihejvioralno uzbuđenje tokom adolescentnog života

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Adolescence is associated with genomically patterned consolidation of the hubs of the human brain connectome

Cited by 481 publications

References 58 publications

Multimodal computational neocortical anatomy in pediatric hippocampal sclerosis

Multimodal computational neocortical anatomy in pediatric hippocampal sclerosis

Large-Scale Gradients in Human Cortical Organization

The adolescent brain: Changes and challenges of development

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