A connectional hub in the rostral anterior cingulate cortex links areas of emotion and cognitive control
- McLean Hospital / Harvard Medical School, United States
- University of Oxford, United Kingdom
- University of Rochester School of Medicine, United States
- Massachusetts General Hospital, United States
Abstract
We investigated afferent inputs from all areas in the frontal cortex (FC) to different subregions in the rostral anterior cingulate cortex (rACC). Using retrograde tracing in macaque monkeys, we quantified projection strength by counting retrogradely labeled cells in each FC area. The projection from different FC regions varied across injection sites in strength, following different spatial patterns. Importantly, a site at the rostral end of the cingulate sulcus stood out as having strong inputs from many areas in diverse FC regions. Moreover, it was at the integrative conjunction of three projection trends across sites. This site marks a connectional hub inside the rACC that integrates FC inputs across functional modalities. Tractography with monkey diffusion magnetic resonance imaging (dMRI) located a similar hub region comparable to the tracing result. Applying the same tractography method to human dMRI data, we demonstrated that a similar hub can be located in the human rACC.
Data availability
All data analysed during this study are included in the manuscript and supporting files. FreeSurfer label files have been provided for Figure 8A.
Article and author information
Author details
Funding
National Institute of Mental Health (MH106435)
- Wei Tang
- Ziyi Zhu
- Julia F Lehman
- Suzanne N Haber
National Institute of Mental Health (MH045573)
- Wei Tang
- Ziyi Zhu
- Julia F Lehman
- Suzanne N Haber
Medical Research Council (MR/L009013/1)
- Saad Jbabdi
National Institute of Mental Health (U01-MH109589)
- Michiel Cottaar
NIH Blueprint for Neuroscience Research (U01-MH093765)
- Giorgia Grisot
- Anastasia Yendiki
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All nonhuman primate experiments were performed in accordance with the Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals and approved by the University Committee on Animal Resources at University of Rochester (Protocol Number UCAR-2008-122R).
Human subjects: The human data were obtained from the publicly available Human Connectome Project database. All procedures conformed to ethical standards approved by the Institutional Review Board of Partners Healthcare. All human subjects have provided written informed consent.
Copyright
© 2019, Tang 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
-
- 4,653
- views
-
- 612
- downloads
-
- 82
- 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)
A connectional hub in the rostral anterior cingulate cortex links areas of emotion and cognitive control
eLife 8:e43761.
https://doi.org/10.7554/eLife.43761
Further reading
-
- Neuroscience
- Stem Cells and Regenerative Medicine
Parkinson’s disease (PD) is a multifactorial disease caused by irreversible progressive loss of dopaminergic neurons (DANs). Recent studies have reported the successful conversion of astrocytes into DANs by repressing polypyrimidine tract binding protein 1 (PTBP1), which led to the rescue of motor symptoms in a chemically-induced mouse model of PD. However, follow-up studies have questioned the validity of this astrocyte-to-DAN conversion model. Here, we devised an adenine base editing strategy to downregulate PTBP1 in astrocytes and neurons in a chemically-induced PD mouse model. While PTBP1 downregulation in astrocytes had no effect, PTBP1 downregulation in neurons of the striatum resulted in the expression of the DAN marker tyrosine hydroxylase (TH) in non-dividing neurons, which was associated with an increase in striatal dopamine concentrations and a rescue of forelimb akinesia and spontaneous rotations. Phenotypic analysis using multiplexed iterative immunofluorescence imaging further revealed that most of these TH-positive cells co-expressed the dopaminergic marker DAT and the pan-neuronal marker NEUN, with the majority of these triple-positive cells being classified as mature GABAergic neurons. Additional research is needed to fully elucidate the molecular mechanisms underlying the expression of the observed markers and understand how the formation of these cells contributes to the rescue of spontaneous motor behaviors. Nevertheless, our findings support a model where downregulation of neuronal, but not astrocytic, PTBP1 can mitigate symptoms in PD mice.
-
- Neuroscience
Organizing the continuous stream of visual input into categories like places or faces is important for everyday function and social interactions. However, it is unknown when neural representations of these and other visual categories emerge. Here, we used steady-state evoked potential electroencephalography to measure cortical responses in infants at 3–4 months, 4–6 months, 6–8 months, and 12–15 months, when they viewed controlled, gray-level images of faces, limbs, corridors, characters, and cars. We found that distinct responses to these categories emerge at different ages. Reliable brain responses to faces emerge first, at 4–6 months, followed by limbs and places around 6–8 months. Between 6 and 15 months response patterns become more distinct, such that a classifier can decode what an infant is looking at from their brain responses. These findings have important implications for assessing typical and atypical cortical development as they not only suggest that category representations are learned, but also that representations of categories that may have innate substrates emerge at different times during infancy.
