Sulcal organization in the medial frontal cortex provides insights into primate brain evolution

Amiez, Céline; Sallet, Jérôme; Hopkins, William D.; Meguerditchian, Adrien; Hadj-Bouziane, Fadila; Hamed, Suliann Ben; Wilson, Charles R.E.; Procyk, Emmanuel; Petrides, Michael

doi:10.1038/s41467-019-11347-x

Cited by 103 publications

(142 citation statements)

References 55 publications

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“…Our results converge with previous research demonstrating differences in local folding patterns in cingulate and temporal regions 9 , 10 , 37 , 52 and empirically integrates these spatially localized differences in support of hypotheses of aberrant fronto-temporal and salience network connectivity underpinning the experience of hallucinations in schizophrenia 15 – 17 , 53 . We advance prior research on sulcal asymmetries in the general population and in developmental and psychiatric disorders 21 , 25 – 28 , 30 , 36 , showing a reduction of the typical leftward PCS asymmetry in schizophrenia patients with hallucinations, due to a shorter left hemisphere PCS, compared to patients without hallucinations and to healthy controls. The rightward STS asymmetry was also lower, with a significantly diminished mean depth of the right STS in H+ patients compared to HCs.…”

Section: Discussionsupporting

confidence: 54%

“…The PCS has consistently been characterized to show a leftward asymmetry, wherein it is more often prominent or present in the left hemisphere than in the right 25 , 36 , 42 . This leftward asymmetry is reduced in patients with schizophrenia 26 – 28 .…”

Section: Methodsmentioning

confidence: 99%

“…The paracingulate sulcus (PCS) is a complex structure on the medial prefrontal cortical surface, found only in humans and chimpanzees 25 , that lies dorsal to the cingulate sulcus. It is characterized by high inter-individual and inter-hemispheric variability, including fragmentation, intersection by other sulci, and even absence (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia

et al. 2020

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All perception is a construction of the brain from sensory input. Our first perceptions begin during gestation, making fetal brain development fundamental to how we experience a diverse world. Hallucinations are percepts without origin in physical reality that occur in health and disease. Despite longstanding research on the brain structures supporting hallucinations and on perinatal contributions to the pathophysiology of schizophrenia, what links these two distinct lines of research remains unclear. Sulcal patterns derived from structural magnetic resonance (MR) images can provide a proxy in adulthood for early brain development. We studied two independent datasets of patients with schizophrenia who underwent clinical assessment and 3T MR imaging from the United Kingdom and Shanghai, China (n = 181 combined) and 63 healthy controls from Shanghai. Participants were stratified into those with (n = 79 UK; n = 22 Shanghai) and without (n = 43 UK; n = 37 Shanghai) hallucinations from the PANSS P3 scores for hallucinatory behaviour. We quantified the length, depth, and asymmetry indices of the paracingulate and superior temporal sulci (PCS, STS), which have previously been associated with hallucinations in schizophrenia, and constructed cortical folding covariance matrices organized by large-scale functional networks. In both ethnic groups, we demonstrated a significantly shorter left PCS in patients with hallucinations compared to those without, and to healthy controls. Reduced PCS length and STS depth corresponded to focal deviations in their geometry and to significantly increased covariance within and between areas of the salience and auditory networks. The discovery of neurodevelopmental alterations contributing to hallucinations establishes testable models for these enigmatic, sometimes highly distressing, perceptions and provides mechanistic insight into the pathological consequences of prenatal origins.

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Section: Discussionsupporting

confidence: 54%

Section: Methodsmentioning

confidence: 99%

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Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia

et al. 2020

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“…The mechanisms of brain folding are not fully understood 19,20 , but the process is largely preserved among humans and non-human primates. The pattern of brain gyri (or sulci) tend to delimit areas with specific functions and are generally consistent across subjects [21][22][23][24] . The complexity and inter-subject variability of brain gyrification are influenced by many factors, including genetically and environmentally influenced developmental, aging and pathological processes 25,26 .…”

Section: Introductionmentioning

confidence: 99%

The reliability and heritability of cortical folds and their genetic correlations across hemispheres

Pizzagalli¹,

Auzias²,

Yang³

et al. 2019

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The structure of the brain's cortical folds varies considerably in human populations. Specific patterns of cortical variation arise with development and aging, and cortical traits are partially influenced by genetic factors. The degree to which genetic factors affect cortical folding patterning remains unknown, yet may be estimated with large-scale in-vivo brain MRI. Using multiple MRI datasets from around the world, we estimated the reliability and heritability of sulcal morphometric characteristics including length, depth, width, and surface area, for 61 sulci per hemisphere of the human brain. Reliability was assessed across four distinct test-retest datasets. We meta-analyzed the heritability across three independent family-based cohorts (N > 3,000), and one cohort of largely unrelated individuals (N~9,000) to examine the robustness of our findings. Reliability was high ( interquartile range for ICC: 0.65-0.85) for sulcal metrics. Most sulcal measures were moderately to highly heritability (0.3-0.7). These genetic influences vary regionally, with the earlier forming sulci having higher heritability estimates. The central sulcus, the subcallosal and the collateral fissure were the most highly heritable regions. For some frontal and temporal sulci, left and right genetic influences did not completely overlap, suggesting some lateralization of genetic effects on the cortex.

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“…In comparative neuroimaging, structural MRI technology has been used to conduct various cross-species comparisons of macrostructures, such as the size of areas and volumes of brain regions (Croxson et al, 2018;Donahue et al, 2018;Eichert et al, 2020;Gomez-Robles et al, 2015;Rilling and Insel, 1999;Rilling and Seligman, 2002;Semendeferi and Damasio, 2000), cortical folding (gyrification) (Amiez et al, 2019;Avants et al, 2006;Glasser et al, 2014;Hopkins et al, 2017;Rilling and Insel, 1999;Van Essen and Dierker, 2007), expansion of cortical areas (Eichert et al, 2020;Hill et al, 2010;Orban et al, 2004;Van Essen and Dierker, 2007), white matter connectivity (Croxson et al, 2018;Reid et al, 2016), and development and aging of the brain (Amlien et al, 2014;Chaplin et al, 2013;Chen et al, 2013;Sakai et al, 2013;Sakai et al, 2011;Sherwood et al, 2011).…”

Section: Role Of Brain Mri In Primate Comparative Neuroscience and Cumentioning

confidence: 99%

The Japan Monkey Centre Primates Brain Imaging Repository of high-resolution postmortem magnetic resonance imaging: the second phase of the archive of digital records

Sakai

Hata

Shintaku

et al. 2020

Preprint

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A comparison of neuroanatomical features of the brain between humans and our evolutionary relatives, nonhuman primates, is key to understanding the human brain system and the neural basis of mental and neurological disorders. Although most comparative MRI studies of human and nonhuman primate brains have been based on brains of primates that had been used as subjects in experiments, it is essential to investigate various species of nonhuman primates in order to elucidate and interpret the diversity of neuroanatomy features among humans and nonhuman primates. To develop a research platform for this purpose, it is necessary to harmonize the scientific contributions of studies with the standards of animal ethics, animal welfare, and the conservation of brain information for long-term continuation of the field. In previous research, we first developed an open-resource repository of anatomical images obtained using 9.4-T ex vivo MRI of postmortem brain samples from 12 nonhuman primate species, and which are stored at the Japan Monkey Centre. In the present study, as a second phase, we released a collection of T2-weighted images and diffusion tensor images obtained in nine species: white-throated capuchin, Bolivian squirrel monkey, stump-tailed macaque, Tibet monkey, Sykes’ monkey, Assamese macaque, pig-tailed macaque, crested macaque, and chimpanzee. Our image repository should facilitate scientific discoveries in the field of comparative neuroscience. This repository can also promote animal ethics and animal welfare in experiments with nonhuman primate models by optimizing methods for in vivo and ex vivo MRI scanning of brains and supporting veterinary neuroradiological education. In addition, the repository is expected to contribute to conservation, preserving information about the brains of various primates, including endangered species, in a permanent digital form.

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Sulcal organization in the medial frontal cortex provides insights into primate brain evolution

Cited by 103 publications

References 55 publications

Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia

Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia

The reliability and heritability of cortical folds and their genetic correlations across hemispheres

The Japan Monkey Centre Primates Brain Imaging Repository of high-resolution postmortem magnetic resonance imaging: the second phase of the archive of digital records

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