Methodological considerations for developmental longitudinal fMRI research

Telzer, Eva H.; McCormick, Ethan M.; Peters, Susan; Cosme, Danielle; Pfeifer, Jennifer H.; Duijvenvoorde, Anna C. K. van

doi:10.1016/j.dcn.2018.02.004

Cited by 81 publications

(77 citation statements)

References 73 publications

(94 reference statements)

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“…For age, we explored both linear and nonlinear, quadratic models as previous studies have demonstrated both linear and nonlinear developmental trajectories in the brain [Telzer et al, 2018]. Figure 2 shows the inverted curvilinear relationship between age and percent signal change in four of the six insular subdivisions.…”

Section: Cardiac Interoceptive Accuracymentioning

confidence: 99%

Neural Correlates of Cardiac Interoceptive Focus Across Development: Implications for Social Symptoms in Autism Spectrum Disorder

et al. 2020

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Interoception involves the processing of sensory information relevant to physiological functioning and is integral to building self‐awareness, emotional states, and modulating social behaviors. With the role of interoception in emotional processing and social functioning, there is growing interest in characterizing interoception in autism spectrum disorder (ASD), yet, there are mixed results regarding cardiac interoceptive accuracy in ASD. In this study, we explored the neural basis of cardiac interoception using an fMRI heartbeat‐counting task in order to assess neural correlates of primary interoception. We predicted that interoceptive‐specific response in the insula, a “hub” for interoception, would be related to ASD symptomatology. We investigated the relationship of insula responses during cardiac interoceptive focus and a self/caregiver‐reported autism‐related symptom scale (Social Responsiveness Scale‐2 (SRS)). Participants included 46 individuals with autism spectrum disorder (ASD) (age 8–54, mean = 19.43 ± 10.68 years) and 54 individuals with typical development for comparison (TC, age 8–53, mean = 21.43 ± 10.41 years). We found no significant difference in cardiac interoceptive accuracy or neural response to cardiac interoception focus in ASD. Several insula subdivisions had a curvilinear relationship to age, peaking in early adulthood. Interoceptive‐specific insula response was associated with adult self‐report SRS scores; this association differed by diagnostic group and was not present for caregiver‐reported scores. This work suggests that (a) there is no global deficit in cardiac interoception in ASD, but integrating interoceptive cues with social information may distinguish individuals with ASD, and (b) there is a developmental trajectory for interoceptive processing in the insula that may be relevant for socio‐emotional health. Autism Res 2020, 13: 908‐920. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. Lay Summary We use internal sensory information from the body, such as signals from the heart, to understand our emotional response to the external world. We measured how accurately people with autism feel their heartbeat and how the brain responds to this type of information. We found no differences between the autism and comparison groups in how the brain senses heartbeats, or in how accurately people feel their heartbeats. However, for people with autism, brain responses while sensing heartbeats were related to social difficulties. This work suggests people with autism may use internal and external information in a different way.

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Section: Cardiac Interoceptive Accuracymentioning

confidence: 99%

Neural Correlates of Cardiac Interoceptive Focus Across Development: Implications for Social Symptoms in Autism Spectrum Disorder

et al. 2020

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“…It is particularly relevant to consider these transformations not only in relation to neural structural or localized activation changes, but also in relation to functional connectivity changes in the adolescent brain (Casey, ; Crone & Dahl, ; Stevens, ). Relative to studies examining structural (Tamnes et al, ) and functional (Telzer et al, ) brain development, very few studies have examined longitudinal functional connectivity changes. The goal of this study was therefore to analyze within and between subcortical–cortical connectivity in participants ages 8–29 years, using a three‐wave longitudinal design covering 5 years for each individual.…”

Section: Introductionmentioning

confidence: 99%

A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

Duijvenvoorde

Westhoff

Vos

et al. 2019

Human Brain Mapping

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Adolescence is the transitional period between childhood and adulthood, characterized by substantial changes in reward‐driven behavior. Although reward‐driven behavior is supported by subcortical‐medial prefrontal cortex (PFC) connectivity, the development of these circuits is not well understood. Particularly, while puberty has been hypothesized to accelerate organization and activation of functional neural circuits, the relationship between age, sex, pubertal change, and functional connectivity has hardly been studied. Here, we present an analysis of resting‐state functional connectivity between subcortical structures and the medial PFC, in 661 scans of 273 participants between 8 and 29 years, using a three‐wave longitudinal design. Generalized additive mixed model procedures were used to assess the effects of age, sex, and self‐reported pubertal status on connectivity between subcortical structures (nucleus accumbens, caudate, putamen, hippocampus, and amygdala) and cortical medial structures (dorsal anterior cingulate, ventral anterior cingulate, subcallosal cortex, frontal medial cortex). We observed an age‐related strengthening of subcortico‐subcortical and cortico‐cortical connectivity. Subcortical–cortical connectivity, such as, between the nucleus accumbens—frontal medial cortex, and the caudate—dorsal anterior cingulate cortex, however, weakened across age. Model‐based comparisons revealed that for specific connections pubertal development described developmental change better than chronological age. This was particularly the case for changes in subcortical–cortical connectivity and distinctively for boys and girls. Together, these findings indicate changes in functional network strengthening with pubertal development. These changes in functional connectivity may maximize the neural efficiency of interregional communication and set the stage for further inquiry of biological factors driving adolescent functional connectivity changes.

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“…Here, we charted adolescent changes in structural connectome organization, based on an accelerated longitudinal neuroimaging study (n = 208) 20,60 . Compared to cross-sectional designs, longitudinal studies track within-subject change, separating developmental effects from between-subject variability [61][62][63][64][65] . Leveraging connectome-wide manifold learning techniques 42 , we first estimated longitudinal changes in structural connectome manifolds across age in a compact and lower dimensional analytical space.…”

Section: Introductionmentioning

confidence: 99%

An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

Park

Bethlehem

Paquola

et al. 2020

Preprint

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Adolescence is a critical time for the continued maturation of brain networks, and the current work assessed longitudinal reconfigurations of diffusion MRI derived connectomes in a large sample (n = 208). We identified an expansion of structural network representations in lower dimensional manifold spaces, with strongest effects in transmodal cortices and indicative of an increasing differentiation of these networks from the rest of the brain. Findings were shown to relate to mainly an increase in within-module connectivity and increased segregation during adolescence. Connectome findings were consistent when additionally controlling for regional changes in MRI measures of cortical morphology and myelin, despite reductions in effect sizes. On the other hand, cortical areas showing manifold expansion were found to become more closely embedded with subcortical targets, notably the striatum. Identified networks were also found to harbor genes significantly expressed in both cortical and subcortical regions. Using supervised machine learning with cross-validation, we demonstrated that cortico-subcortical manifold features at baseline and their maturational change predicted measures of intelligence at follow-up. Our findings chart adolescent connectome development and suggest that brain-wide network reconfigurations offer intermediary phenotypes between genetic-microstructural processes and cognitive-behavioral outcomes.We explored how whole-brain structural networks reconfigure during adolescence, using a novel analysis that simultaneously interrogates network and regional features. Our approach revealed an increasing differentiation of the connectome during this critical period, particularly in higher-order prefrontal and parietal regions. We could show that while this effect was only partially related to developmental trajectories of intracortical microstructure and morphology, but rather to changes in connectivity to subcortical areas, particularly the striatum. Cortico-subcortical network effects were also supported by transcriptomics and phenotype prediction, which suggested that cognitive function in adulthood was most effectively predicted when combining cortical and subcortical features. Our findings shed new light on adolescence and support a key role of cortico-subcortical integration in shaping macroscale structural networks. Park et al. | Structural connectome maturation during adolescence 3 3

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Methodological considerations for developmental longitudinal fMRI research

Cited by 81 publications

References 73 publications

Neural Correlates of Cardiac Interoceptive Focus Across Development: Implications for Social Symptoms in Autism Spectrum Disorder

Neural Correlates of Cardiac Interoceptive Focus Across Development: Implications for Social Symptoms in Autism Spectrum Disorder

A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

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