Cited by 833Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationPrimate Behavior and Ecology

Modeling transformations of neurodevelopmental sequences across mammalian species

Open access
Workman, Alan D., Charvet, Christine J., Clancy, Barbara, Darlington, Richard B., Finlay, Barbara L.·2013·The Journal of Neuroscience

Abstract

A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1523/jneurosci.5746-12.2013

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • A study of protein expression in human female fetuses with and without trisomy (n = 4 each) at gestational week 18-19 found no differences in protein expression.

    “Notably, a study of protein expression in human female fetuses with and without trisomy (n = 4 each) at gestational week 18–19, a stage of human brain development that is roughly equivalent to the late fetal period in mouse brain development (Workman et al., 2013), found no differences in protein expression (Cheon et al., 2003).”

    From Sex-specific developmental alterations in DYRK1A expression in the brain of a Down syndrome mouse model (2024) · cites this paper as Workman et al., 2013

    The Workman citation is attached to the human–mouse developmental-stage comparison, not to the protein-expression finding, which the sentence cites to Cheon et al. In “Slope and onset of progression through neural events” (page unavailable), Workman et al. compare the timing of neural milestones across species, but the passages found do not establish that human gestational weeks 18–19 specifically correspond to the late fetal period in mice. (LLM, conf=0.76)

    Experimental — accuracy not yet measured
  • These significant and large increases in DYRK1A expression suggest that P6 may be a time of excessive DYRK1A kinase activity that alters the trajectory of the trisomic brain at a critical period of its development.

    “These significant and large increases in DYRK1A expression suggest that P6—roughly equivalent to the period of human brain development in the early third trimester (Workman et al., 2013)— may be a time of excessive DYRK1A kinase activity that alters the trajectory of the trisomic brain at a critical period of its development.”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 37

  1. Brooksbank BW, Walker D, Bala ´zs R, Jørgensen OS (1989) Neuronal mat- uration in the foetal brain in Down's syndrome. Early Hum Dev 18:237- 246. CrossRef Medline · DOI
  2. Bryden MM, Evans HE, Binns W (1972) Embryology of the sheep. I. Extra- embryonic membranes and the development of body form. J Morphol 138:169 -185. CrossRef Medline · DOI
  3. Caviness VS Jr, Lange NT, Makris N, Herbert MR, Kennedy DN (1999) MRI-based brain volumetrics: emergence of a developmental brain sci- ence. Brain Dev 21:289 -295. CrossRef Medline · DOI
  4. Chalupa LM, Williams RW (2008) Eye, retina and visual system of the mouse. Cambridge, Massachusetts: MIT
  5. Charvet CJ, Finlay BL (2012) Embracing covariation in brain evolution: large brains, extended development and flexible primate social systems. Prog Brain Res 195:71-87. CrossRef Medline · DOI
  6. Charvet CJ, Sandoval AL, Striedter GF (2010) Phylogenetic origins of early alterations in brain region proportions. Brain Behav Evol 75:104 -110. CrossRef Medline · DOI
  7. Clancy B, Darlington RB, Finlay BL (2000) The course of human events: predicting the timing of primate neural development. Dev Sci 3:57-66. CrossRef · DOI
  8. Clark DA, Mitra PP, Wang SS (2001) Scalable architecture in mammalian brains. Nature 411:189 -193. CrossRef Medline · DOI · Paper page
  9. Darlington RB (1990) Regression and linear models. New York: McGraw- Hill
  10. Darlington RB, Dunlop SA, Finlay BL (1999) Neural development in metatherian and eutherian mammals: variation and constraint. J Comp Neurol 411:359 -368. CrossRef Medline · DOI
  11. de Winter W, Oxnard CE (2001) Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409:710 -714. CrossRef Medline · DOI · Paper page
  12. Dreher B, Robinson SR (1988) Development of the retinofugal pathway in birds and mammals: evidence for a common timetable. Brain Behav Evol 31:369 -390. CrossRef Medline · DOI
  13. Dunbar RI, Shultz S (2007) Evolution in the social brain. Science 317:1344 - 1347. CrossRef Medline · DOI
  14. Dyer MA, Martins R, da Silva Filho M, Muniz JA, Silveira LC, Cepko CL, Finlay BL (2009) Developmental sources of conservation and variation in the evolution of the primate eye. Proc Natl Acad Sci U S A 106:8963- 8968. CrossRef Medline · DOI
  15. Finlay, BL, Clancy B (2008) Chronology of the development of the mouse visual system. In: Eye, retina and visual system of the mouse (Chalupa L, Williams RW, eds), pp 257-265. Cambridge, MA: MIT.
  16. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578 -1584. CrossRef Medline · DOI · Paper page
  17. Finlay BL, Hersman MN, Darlington RB (1998) Patterns of vertebrate neu- rogenesis and the paths of vertebrate evolution. Brain Behav Evol 52:232- 242. CrossRef Medline · DOI
  18. Flatt T, Heyland A (2011) Mechanisms of life history evolution. Oxford, UK: Oxford UP
  19. Garcia-Lopez R, Pombero A, Martinez S (2009) Fate map of the chick em- bryo neural tube. Dev Growth Differ 51:145-165. CrossRef Medline · DOI
  20. Gould SJ (1977) Ontogeny and phylogeny. Cambridge, Massachusetts: Harvard UP
  21. Iwaniuk AN, Dean KM, Nelson JE (2004) A mosaic pattern characterizes the evolution of the avian brain. Proc Biol Sci 271[Suppl4]:S148 -151. CrossRef Medline · DOI · Paper page
  22. Kingsbury MA, Gleason ED, Ophir AG, Phelps SM, Young LJ, Marler CA (2012) Monogamous and promiscuous rodent species exhibit discrete variation in the size of the medial prefrontal cortex. Brain Behav Evol 80:4 -14. CrossRef Medline · DOI
  23. Kostovic I, Rakic P (1980) Cytology and time of origin of interstitial neu- rons in the white matter in infant and adult human and monkey telen- cephalon. J Neurocytol 9:219 -242. CrossRef Medline · DOI
  24. Le Magueresse C, Monyer H (2013) GABAergic interneurons shape the functional maturation of the cortex. Neuron 77:388 -405. CrossRef Medline · DOI · Paper page
  25. Lumsden A (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 13:329 -335. CrossRef Medline · DOI
  26. Lumsden A (2004) Segmentation and compartition in the early avian hind- brain. Mech Dev 121:1081-1088. CrossRef Medline · DOI
  27. Passingham RE (1985) Rates of brain development in mammals including man. Brain Behav Evol 26:167-175. CrossRef Medline · DOI
  28. Puelles L (1995) A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav Evol 46:319 -337. CrossRef Medline · DOI
  29. Puelles L, Rubenstein JL (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469 -476. CrossRef Medline · DOI · Paper page
  30. Raznahan A, Greenstein D, Lee NR, Clasen LS, Giedd JN (2012) Prenatal growth in humans and postnatal brain maturation into late adolescence. Proc Natl Acad Sci U S A 109:11366 -11371. CrossRef Medline · DOI
  31. Reep RL, Darlington RB, Finlay BL (2007) The limbic system in mammalian brain evolution. Brain Behav Evol 70:57-70. CrossRef Medline · DOI
  32. Robson SL, van Schaik CP, Hawkes K (2006) The derived features of human life history. In: The evolution of human life history (Hawkes K, Paine RR), pp. 17-44. Santa Fe, NM: School of American Research
  33. Ross CF, Kirk EC (2007) Evolution of eye size and shape in primates. J Hum Evol 52:294 -313. CrossRef Medline · DOI
  34. Schuppli C, Isler K, van Schaik CP (2012) How to explain the unusually late age at skill competence among humans. J Hum Evol 63:843-850. CrossRef Medline · DOI
  35. Song S, Liu L, Edwards SV, Wu S (2012) Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proc Natl Acad Sci U S A 109:14942-14947. CrossRef Medline · DOI
  36. Stevens CF (2001) An evolutionary scaling law for the primate visual system and its basis in cortical function. Nature 411:193-195. CrossRef Medline · DOI
  37. Yopak KE, Lisney TJ, Darlington RB, Collin SP, Montgomery JC, Finlay BL (2010) A conserved pattern of brain scaling from sharks to primates. Proc Natl Acad Sci U S A 107:12946 -12951. CrossRef Medline · DOI

Cited by

Sorted by citations

Authors
Workman, A. D., Charvet, C. J., Clancy, B., Darlington, R. B., & Finlay, B. L.
Affiliations
  • Cornell University (US)
  • University of Central Arkansas (US)
Venue
The Journal of Neuroscience
Published
2013-04-24
Volume
33
Issue
17
Pages
7368-7383
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2022567100
Cited by
833
References
5
Citations by year
2026: 48 · 2025: 82 · 2024: 46 · 2023: 59 · 2022: 65 · 2021: 76 · 2020: 76 · 2019: 68 · 2018: 74 · 2017: 60 · 2016: 76 · 2015: 48 · 2014: 34 · 2013: 21
FWCI
22.15
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (0849627, 0849612)
  • National Institutes of Health
  • U.S. Public Health Service (NIH CHHD 1F32HD067011-01A1)
  • National Center for Research Resources (P20RR016460, P20 RR 16460)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (F32HD067011, U10 HD-500009)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
Keywords
neural development, brain evolution, heterochrony, developmental timing, neurogenesis, axon growth, myelination, brain growth, retinal development, cortical development, marsupials, rodents, macaque, human development
MeSH terms
Animals, Brain, Cats, Biological Evolution, Ferrets, Gerbillinae, Guinea Pigs, Cricetinae, Humans, Macropodidae, Macaca, Models, Neurological, Rabbits, Sheep, Species Specificity, Trichosurus, Mice, Rats, Neurogenesis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review