Brain Charts for the Rhesus Macaque
Poster No:
1259
Submission Type:
Abstract Submission
Authors:
Samuel Alldritt1, Julian Ramirez1, Jakob Seidlitz2, Richard Bethlehem3, Karl-Heinz Nenning4, David Amaral5, Damien Fair6, Andrew Fox7, Alexandre Franco4, Jeff Bennett8, Ned Kalin9,10, Brian Russ4, Lena Dorfschmidt11, Aaron Alexander-Bloch2, Daniel Margulies12, Jonathan Smallwood13, Charles Schroeder14, Becker Guillaume15, Mar Sanchez16, Lucie Chalet17, Daniel Gale13, Zsofie Kovacs-Balint18, Jason Gallivan19, Joseph Nashed20, Clement Garin21, John Erdman22, Matthew Kuchan23, Martha Neuringer24, Viola Neudecker25, Oscar Miranda Dominguez26, Ansgar Brambrink25, Christopher Kroenke24, Christopher Petkov27, Jiaojing Wang28, Chris Klink29, Adam Messinger30, PRIME-DE Consortium1, Michael Milham1, Ting Xu1
Institutions:
1Child Mind Institute, New York, NY, 2University of Pennsylvania, Philadelphia, PA, 3Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom, 4Nathan Kline Institute, Orangeburg, NY, 5University of California Davis MIND Institute, Sacramento, CA, 6Masonic Institute for the Developing Brain, University of Minnesota Medical School, Minneapolis, MN, 7University of California Davis, Davis, CA, 8California National Primate Research Center, Davis, CA, 9University of Wisconsin Madison, Madison, WI, 10Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, WI, 11The Children’s Hospital of Philadelphia, Philadelphia, PA, 12Université Paris Cité, CNRS, Integrative Neuroscience and Cognition Center, Paris, France, 13Department of Psychology, Queen’s University, Ontario, Canada, 14Nathan S. kline Institute for Psychiatric Research, Orangeburg, NY, 15Université de Lyon, Lyon, France, 16Emory National Primate Research Center, Atlanta, GA, 17Claude Bernard University Lyon 1, Villeurbanne, France, 18Emory University, Budapest, Hungary, 19Department of Psychology, Queens University, Ontario, Canada, 20Centre for Neuroscience Studies, Queen’s University, Ontario, Canada, 21Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 22Beckman Institute for Advanced Science and Technology, Champaign, IL, 23Abbott Laboratories, Columbus, OH, 24Oregon National Primate Research Center, Portland, OR, 25Columbia University, New York, NY, 26University of Minnesota, Minneapolis, MN, 27Newcastle University, Newcastle, United Kingdom, 28Kunming University of Science and Technology, Kunming, China, 29Netherlands Institute for Neuroscience Royal Netherlands Academy of Arts and Sciences, Meibergdreef, Netherlands, 30National Institute of Health, Baltimore, MD
First Author:
Co-Author(s):
Richard Bethlehem
Autism Research Centre, Department of Psychiatry, University of Cambridge
Cambridge, United Kingdom
Autism Research Centre, Department of Psychiatry, University of Cambridge
Cambridge, United Kingdom
Damien Fair
Masonic Institute for the Developing Brain, University of Minnesota Medical School
Minneapolis, MN
Masonic Institute for the Developing Brain, University of Minnesota Medical School
Minneapolis, MN
Ned Kalin
University of Wisconsin Madison|Department of Psychiatry, University of Wisconsin School of Medicine and Public Health
Madison, WI|Madison, WI
University of Wisconsin Madison|Department of Psychiatry, University of Wisconsin School of Medicine and Public Health
Madison, WI|Madison, WI
Daniel Margulies
Université Paris Cité, CNRS, Integrative Neuroscience and Cognition Center
Paris, France
Université Paris Cité, CNRS, Integrative Neuroscience and Cognition Center
Paris, France
Chris Klink
Netherlands Institute for Neuroscience Royal Netherlands Academy of Arts and Sciences
Meibergdreef, Netherlands
Netherlands Institute for Neuroscience Royal Netherlands Academy of Arts and Sciences
Meibergdreef, Netherlands
Introduction:
The rhesus macaque is one of the most widely used non-human primate (NHP) models for the human brain, due to resemblance in brain structure, function, and social behaviours. Notably, comparative developmental models of human and macaque provides opportunities to investigate neural plasticity, developmental trajectories, and pathological processes. Recently, analysis of multisite MRI datasets have successfully characterized human brain development across the lifespan [1]. However, due to multifaceted challenges in NHP studies, we lack comparative brain growth charts for macaques. This study aimed to establish reference standards for macaque brain development that facilitates the comparison of development phases across humans and macaques.
Methods:
We studied a collaborative multisite collection of MRI data including the PRIMatE Data Exchange (PRIME-DE) consortium. Structural images were preprocessed through the 'nhp-abcd-bids-pipeline'[2-4], with customized templates for early developmental data (age < 0.3 yr), followed by visual inspections for quality assessment. Prenatal data was manually segmented [5]. A total of 1,522 scans (1024 macaques, 554 F, age: -.23 - 30.64 yr) across 23 sites were included in the analysis. We estimated global and regional volume, cortical thickness, and surface area and applied a GAMLSS, fitting nonlinear growth curves stratified by sex and site as a random effect. We identified the macaque developmental milestones (i.e. growth rates and peak age of trajectories) and transformed them to human surfaces for comparing the developmental phases between humans and macaques.
Results:
Overall, macaque trajectories demonstrate similar patterns in total volume of gray matter (GMV), white matter, and subcortical GM compared to humans. However, unlike humans, where GMV peaks in childhood (~6 yr), macaque GMV peaked earlier during infancy (~8 mon), followed by a plateau and gradual decline. Ventricular volume sharply decreases before birth, with a steady postnatal increase, followed by a slight increase towards the end of the lifespan. At the GMV peak age (Fig 1C), the growth rate in volume, area, and cortical thickness shows regional variations [6]. Except for the frontal pole, volumes in the lateral and medial frontal, middle temporal, and parahippocampal regions continue to increase, while the visual and parietal lobes show a reduction. Cortical thickness mirrors a similar pattern to volume, while surface area displays continued expansion in most brain regions, except for the visual cortex.
Figure 2 illustrates regional peak ages for volume, area, and thickness. Notably, volume and area share a similar peak age scale across regions, with a late peak age observed in the precentral gyrus and anterior cingular cortex (ACC). In contrast, thickness exhibits an earlier overall peak age. Upon comparing the human peak age with that of macaque transformed on the human surface (Fig 2C-D), a development delay was detected in the insular and ACC across all measures (Fig 2F), highlighting functional relationships including social cognition, autobiographical memory, and affective processing.
Figure 2 illustrates regional peak ages for volume, area, and thickness. Notably, volume and area share a similar peak age scale across regions, with a late peak age observed in the precentral gyrus and anterior cingular cortex (ACC). In contrast, thickness exhibits an earlier overall peak age. Upon comparing the human peak age with that of macaque transformed on the human surface (Fig 2C-D), a development delay was detected in the insular and ACC across all measures (Fig 2F), highlighting functional relationships including social cognition, autobiographical memory, and affective processing.
Conclusions:
This study established normative brain development trajectories for macaque. Compared to human, macaque brain grows faster and plateaus earlier, particularly in regions with functional associations with social cognition, autobiographical memory, and affective processing. Our findings suggest neotenic changes in human brain development with prolonged periods of postnatal brain growth during childhood, which may facilitate cellular maturation, myelination, synaptic wiring, and pruning. Functionally these changes are important for the development of complex cognitive and social behaviours that are core features of human cognition. The normative brain charts offer a window into the brain development of nonhuman primates that provides a baseline from which we can gain an understanding of how human brain development shapes how we think and feel.
Lifespan Development:
Aging
Early life, Adolescence, Aging 1
Normal Brain Development: Fetus to Adolescence
Neuroanatomy, Physiology, Metabolism and Neurotransmission:
Cortical Anatomy and Brain Mapping 2
Normal Development
Keywords:
Aging
ANIMAL STUDIES
Development
MRI
Multivariate
Open Data
STRUCTURAL MRI
Structures
Sub-Cortical
White Matter
1|2Indicates the priority used for review
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