Cutting across structural and transcriptomic scales translates time across the lifespan and resolves frontal cortex development in human evolution

Mapping Intimacies ◽

10.1101/2020.08.06.240077 ◽

2020 ◽

Author(s):

Christine J. Charvet

Keyword(s):

Prefrontal Cortex ◽

Human Brain ◽

Temporal Variation ◽

Frontal Cortex ◽

Human Cognition ◽

Developmental Programs ◽

Rigorous Approach ◽

Expression Of Genes ◽

Transcriptional Variation ◽

Development And Aging

AbstractHow the unique capacities of human cognition arose in evolution is a question of enduring interest. It is still unclear which developmental programs are responsible for the emergence of the human brain. The inability to determine corresponding ages between humans and apes has hampered progress in detecting developmental programs leading to the emergence of the human brain. I harness temporal variation in anatomical, behavioral, and transcriptional variation to determine corresponding ages from fetal to postnatal development and aging, between humans and chimpanzees. This multi-dimensional approach results in 137 corresponding time points across the lifespan, from embryonic day 44 to ∼55 years of age, in humans and their equivalent ages in chimpanzees. I used these data to test whether developmental programs, such as the timeline of prefrontal cortex maturation, previously claimed to differ between humans and chimpanzees, do so once variation in developmental schedules is controlled for. I compared the maturation of frontal cortex projections from structural magnetic resonance (MR) scans and from temporal variation in the expression of genes used to track long-range projecting neurons (i.e., supragranular-enirhced genes) in chimpanzees and humans. Contrary to what has been suggested, the timetable of prefrontal cortex maturation is not unusually extended in humans. This dataset, which is the largest with which to determine corresponding ages across humans and chimpanzees, provides a rigorous approach to control for variation in developmental schedules and to identify developmental programs responsible for unique features of the human brain.

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Cutting across structural and transcriptomic scales translates time across the lifespan in humans and chimpanzees

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.2987 ◽

2021 ◽

Vol 288 (1944) ◽

pp. 20202987

Author(s):

Christine J. Charvet

Keyword(s):

Prefrontal Cortex ◽

Human Brain ◽

Temporal Variation ◽

Human Cognition ◽

Dimensional Approach ◽

Time Points ◽

Rigorous Approach ◽

Expression Of Genes ◽

Transcriptional Variation ◽

Do So

How the unique capacities of human cognition arose in evolution is a question of enduring interest. It is still unclear which developmental programmes are responsible for the emergence of the human brain. The inability to determine corresponding ages between humans and apes has hampered progress in detecting developmental programmes leading to the emergence of the human brain. I harness temporal variation in anatomical, behavioural and transcriptional variation to determine corresponding ages from fetal to postnatal development and ageing, between humans and chimpanzees. This multi-dimensional approach results in 137 corresponding time points across the lifespan, from embryonic day 44 to approximately 55 years of age, in humans and their equivalent ages in chimpanzees. I used these data to test whether developmental programmes, such as the timeline of prefrontal cortex (PFC) maturation, previously claimed to differ between humans and chimpanzees, do so once variation in developmental schedules is controlled for. I compared the maturation of frontal cortex projections from structural magnetic resonance (MR) scans and from temporal variation in the expression of genes used to track long-range projecting neurons (i.e. supragranular-enriched genes) in chimpanzees and humans. Contrary to what has been suggested, the timetable of PFC maturation is not unusually extended in humans. This dataset, which is the largest with which to determine corresponding ages across humans and chimpanzees, provides a rigorous approach to control for variation in developmental schedules and to identify developmental programmes responsible for unique features of the human brain.

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Is the Human Brain Unique?

10.1093/med/9780190850128.003.0002 ◽

2018 ◽

Author(s):

Jack M. Gorman

Keyword(s):

Prefrontal Cortex ◽

Theory Of Mind ◽

Human Brain ◽

Brain Function ◽

Human Mind ◽

Brain Diseases ◽

Expression Of Genes ◽

The Future ◽

Mind And Brain ◽

The Brain

Some scientists now argue that humans are really not superior to other species, including our nearest genetic neighbors, chimpanzees and bonobos. Indeed, those animals seem capable of many things previously thought to be uniquely human, including a sense of the future, empathy, depression, and theory of mind. However, it is clear that humans alone produce speech, dominate the globe, and have several brain diseases like schizophrenia. There are three possible sources within the brain for these differences in brain function: in the structure of the brain, in genes coding for proteins in the brain, and in the level of expression of genes in the brain. There is evidence that all three are the case, giving us a place to look for the intersection of the human mind and brain: the expression of genes within neurons of the prefrontal cortex.

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Coordinated Gene Expression of Neuroinflammatory and Cell Signaling Markers in Dorsolateral Prefrontal Cortex during Human Brain Development and Aging

PLoS ONE ◽

10.1371/journal.pone.0110972 ◽

2014 ◽

Vol 9 (10) ◽

pp. e110972 ◽

Cited By ~ 23

Author(s):

Christopher T. Primiani ◽

Veronica H. Ryan ◽

Jagadeesh S. Rao ◽

Margaret C. Cam ◽

Kwangmi Ahn ◽

...

Keyword(s):

Gene Expression ◽

Prefrontal Cortex ◽

Human Brain ◽

Cell Signaling ◽

Brain Development ◽

Dorsolateral Prefrontal Cortex ◽

Human Brain Development ◽

Dorsolateral Prefrontal ◽

Development And Aging

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Tracing cortical circuits in humans and non-human primates from high resolution connectomic, transcriptomic, and temporal dimensions

10.1101/2021.04.30.442016 ◽

2021 ◽

Author(s):

Christine J. Charvet ◽

Kwadwo Ofori ◽

Christine Baucum ◽

Jianli Sun ◽

Melinda S. Modrell ◽

...

Keyword(s):

Gene Expression ◽

High Resolution ◽

Human Brain ◽

Frontal Cortex ◽

Neural Circuits ◽

Human Cognition ◽

Biological Organization ◽

Brain Connectome ◽

Temporal Dimensions ◽

Human Primate

AbstractThe neural circuits that support human cognition are a topic of enduring interest. Yet, the lack of tools available to map human brain circuits has precluded our ability to trace the human and non-human primate connectome. We harnessed high-resolution connectomic, anatomic, and transcriptomic data to investigate the evolution and development of frontal cortex circuitry. We applied machine learning to RNA sequencing data to find corresponding ages between humans and macaques and to compare the development of circuits across species. We transcriptionally defined neural circuits by testing for associations between gene expression and white matter maturation. We then considered transcriptional and structural growth to test whether frontal cortex circuit maturation is unusually extended in humans relative to other species. We also considered gene expression and high-resolution diffusion MR tractography of adult brains to test for cross-species variation in frontal cortex circuits. We found that frontal cortex circuitry development is extended in primates, and concomitant with an expansion in cortico-cortical pathways compared with mice in adulthood. Importantly, we found that these parameters varied relatively little across humans and studied primates. These data identify a surprising collection of conserved features in frontal cortex circuits across humans and Old World monkeys. Our work demonstrates that integrating transcriptional and connectomic data across temporal dimensions is a robust approach to trace the evolution of brain connectomics in primates.Significance StatementWe lack appropriate tools to visualize the human brain connectome. We develop new approaches to study connections in the human and non-human primate brains. The integration of transcription with structure offers an unprecedented opportunity to study circuitry evolution. Our integrative approach finds corresponding ages across species and transcriptionally defines neural circuits. We used this information to test for variation in circuit maturation across species and found a surprising constellation of similar features in frontal cortex neural circuits across humans and primates. Integrating across scales of biological organization expands the repertoire of tools available to study connections in primates, which opens new avenues to study connections in health and diseases of the human brain.

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