Using multi-modal neuroimaging to characterise social brain specialisation in infants
- Birkbeck, University of London, United Kingdom
- University of Padova, Italy
- University of Cambridge, United Kingdom
- University College London, United Kingdom
Abstract
The specialised regional functionality of the mature human cortex partly emerges through experience-dependent specialisation during early development. Our existing understanding of functional specialisation in the infant brain is based on evidence from unitary imaging modalities and has thus focused on isolated estimates of spatial or temporal selectivity of neural or haemodynamic activation, giving an incomplete picture. We speculate that functional specialisation will be underpinned by better coordinated haemodynamic and metabolic changes in a broadly orchestrated physiological response. To enable researchers to track this process through development, we develop new tools that allow the simultaneous measurement of coordinated neural activity (EEG), metabolic rate and oxygenated blood supply (broadband near-infrared spectroscopy) in the awake infant. In 4-to-7-month-old infants, we use these new tools to show that social processing is accompanied by spatially and temporally specific increases in coupled activation in the temporal-parietal junction, a core hub region of the adult social brain. During non-social processing coupled activation decreased in the same region, indicating specificity to social processing. Coupling was strongest with high frequency brain activity (beta and gamma), consistent with the greater energetic requirements and more localised action of high frequency brain activity. The development of simultaneous multi-modal neural measures will enable future researchers to open new vistas in understanding functional specialisation of the brain.
Data availability
The data contains human subject data from minors and guardians provided informed consent to having data shared only with researchers involved in the project, in anonymised form. A Patient and Public Involvement (PPI) initiative at the Centre for Brain and Cognitive Development aimed to actively work in partnership with parents and guardians participating in research studies to help design and manage future research. A comprehensive public survey was conducted as part of this initiative which aimed to evaluate parent attitudes to data sharing in developmental science. This survey revealed that majority of parents do not want their data to be shared openly but are open to the data being shared with other researchers related to the project. Therefore, in order to adhere to participant preference/choice, a curated data sharing approach must be followed wherein the data can only be made available upon reasonable request through a formal data sharing and project affiliation agreement. The researcher will have to contact MFS and complete a project affiliation form providing their study aims, a detailed study proposal, plan for the analysis protocol, ethics, and plans for data storage and protection. Successful proposals will have aims aligned with the aims of the original study. Raw NIRS data, EEG data and integrated NIRS-EEG data can be made available in anonymised form. ID numbers linking the NIRS and EEG data, however, cannot be provided as parents/guardians have consented only to data being shared in anonymised form. All code used to analyse the NIRS data and the integration of the NIRS and EEG data is available on GitHub (https://github.com/maheensiddiqui91/NIRS-EEG). EEG data was processed using EEGlab which is a publicly available toolbox.
Article and author information
Author details
Funding
Biotechnology and Biological Sciences Research Council ([BB/J014567/1])
- Maheen Siddiqui
Economic and Social Research Council (ES/V012436/1)
- Maheen Siddiqui
Economic and Social Research Council (ES/R009368/1)
- Maheen Siddiqui
Horizon 2020 Framework Programme (777394)
- Maheen Siddiqui
- Mark H Johnson
- Emily JH Jones
Wellcome Trust (104580/Z/14/Z)
- Ilias Tachtsidis
UK Research and Innovation (MR/S018425/1)
- Sarah Lloyd-Fox
Bill and Melinda Gates Foundation (OPP1127625)
- Sarah Lloyd-Fox
- Clare E Elwell
Medical Research Council (MR/K021389/1,MR/T003057/1)
- Mark H Johnson
- Emily JH Jones
University of Padova (C96C18001930005)
- Sabrina Brigadoi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The study protocol was approved by the Birkbeck Ethics Committee, ethics approval number 161747. Participants were forty-two 4-to-7-month-old infants (mean age: 179{plus minus} 16 days; 22 males and 20 females); parents provided written informed consent to participate in the study, for the publication of the research and additionally for the publication and use of any photographs taken during the study of the infant wearing the NIRS-EEG headgear.
Copyright
© 2023, Siddiqui et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 955
- views
-
- 166
- downloads
-
- 3
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Using multi-modal neuroimaging to characterise social brain specialisation in infants
eLife 12:e84122.
https://doi.org/10.7554/eLife.84122
Further reading
-
- Developmental Biology
Wing dimorphism is a common phenomenon that plays key roles in the environmental adaptation of aphid; however, the signal transduction in response to environmental cues and the regulation mechanism related to this event remain unknown. Adenosine (A) to inosine (I) RNA editing is a post-transcriptional modification that extends transcriptome variety without altering the genome, playing essential roles in numerous biological and physiological processes. Here, we present a chromosome-level genome assembly of the rose-grain aphid Metopolophium dirhodum by using PacBio long HiFi reads and Hi-C technology. The final genome assembly for M. dirhodum is 447.8 Mb, with 98.50% of the assembled sequences anchored to nine chromosomes. The contig and scaffold N50 values are 7.82 and 37.54 Mb, respectively. A total of 18,003 protein-coding genes were predicted, of which 92.05% were functionally annotated. In addition, 11,678 A-to-I RNA-editing sites were systematically identified based on this assembled M. dirhodum genome, and two synonymous A-to-I RNA-editing sites on CYP18A1 were closely associated with transgenerational wing dimorphism induced by crowding. One of these A-to-I RNA-editing sites may prevent the binding of miR-3036-5p to CYP18A1, thus elevating CYP18A1 expression, decreasing 20E titer, and finally regulating the wing dimorphism of offspring. Meanwhile, crowding can also inhibit miR-3036-5p expression and further increase CYP18A1 abundance, resulting in winged offspring. These findings support that A-to-I RNA editing is a dynamic mechanism in the regulation of transgenerational wing dimorphism in aphids and would advance our understanding of the roles of RNA editing in environmental adaptability and phenotypic plasticity.
-
- Developmental Biology
CDK8 and CDK19 paralogs are regulatory kinases associated with the transcriptional Mediator complex. We have generated mice with the systemic inducible Cdk8 knockout on the background of Cdk19 constitutive knockout. Cdk8/19 double knockout (iDKO) males, but not single Cdk8 or Cdk19 KO, had an atrophic reproductive system and were infertile. The iDKO males lacked postmeiotic spermatids and spermatocytes after meiosis I pachytene. Testosterone levels were decreased whereas the amounts of the luteinizing hormone were unchanged. Single-cell RNA sequencing showed marked differences in the expression of steroidogenic genes (such as Cyp17a1, Star, and Fads) in Leydig cells concomitant with alterations in Sertoli cells and spermatocytes, and were likely associated with an impaired synthesis of steroids. Star and Fads were also downregulated in cultured Leydig cells after iDKO. The treatment of primary Leydig cell culture with a CDK8/19 inhibitor did not induce the same changes in gene expression as iDKO, and a prolonged treatment of mice with a CDK8/19 inhibitor did not affect the size of testes. iDKO, in contrast to the single knockouts or treatment with a CDK8/19 kinase inhibitor, led to depletion of cyclin C (CCNC), the binding partner of CDK8/19 that has been implicated in CDK8/19-independent functions. This suggests that the observed phenotype was likely mediated through kinase-independent activities of CDK8/19, such as CCNC stabilization.
