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Developmental Sequences Predict Increased Connectivity in Brain Evolution: A Comparative Analysis of Developmental Timing, Gene Expression, Neuron Numbers, and Diffusion MR Tractography

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Abstract

A conserved sequence in cell-type specification across mammals suggests that evolutionary changes in developmental timing may give rise to predictable changes in connectivity patterns across species. We here review the regularities in the timing of developmental events across species. We then use them to predict evolutionary changes in the number of cell types in order to identify evolutionary changes in the internal circuitry of the cerebellum as well as the gray and white matter of the isocortex across mammals. We survey what is known about the sequence and timing of cell-type specification in different brain regions and in various mammalian species. We find that lengthened developmental schedules predict a disproportionate increase in the number of locally projecting granule cells within the cerebellum and in the number of isocortical neurons projecting within or across cortical areas. Our main conclusion is that, as brains get bigger, neurons increasingly connect within their own major brain region.

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References

  • Andersen BB, Korbo L, Pakkenberg B (1992) A quantitative study of the human cerebellum with unbiased stereological techniques. J Comp Neurol 326:549–560

    Article  CAS  PubMed  Google Scholar 

  • Barbas H (1986) Pattern in the laminar origin of corticocortical connections. J Comp Neurol 252:415–422

    Article  CAS  PubMed  Google Scholar 

  • Bassett DS, Bullmore ED (2006) Small-world brain networks. Neuroscientist 12:512–523

    Article  PubMed  Google Scholar 

  • Bayer SA, Altman J (1991) Neocortical development. Raven Press, New York

    Google Scholar 

  • Belgard TG, Marques AC, Oliver PL et al (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71:605–616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349

    CAS  PubMed  Google Scholar 

  • Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9:110–122

    Article  CAS  PubMed  Google Scholar 

  • Cahalane DJ, Charvet CJ, Finlay BL (2012) Systematic, balancing gradients in neuron density and number across the primate isocortex. Front Neuroanat 6:28

    Article  PubMed  PubMed Central  Google Scholar 

  • Cahalane DJ, Charvet CJ, Finlay BL (2014) Modeling local and cross-species neuron number variations in the cerebral cortex as arising from a common mechanism. Proc Natl Acad Sci U S A 111:17642–17647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charvet CJ, Finlay BL (2012) Embracing covariation in brain evolution: large brains, extended development, and flexible primate social systems. Prog Brain Res 195:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Charvet CJ, Hof PR, Raghanti MA, Van Der Kouwe AJ, Sherwood CC, Takahashi E (2017a) Combining diffusion magnetic resonance tractography with stereology highlights increased cross-cortical integration in primates. J Comp Neurol 525:1075–1093

    Google Scholar 

  • Charvet CJ, Stimpson CD, Kim YD, Raghanti MA, Lewandowski AH, Hof PR, Gomez-Robles A, Krienen FM, Sherwood CC (2017b) Gradients in cytoarchitectural landscapes of the isocortex: Diprotodont marsupials in comparison to eutherian mammals. J Comp Neurol 525:1811–1826

    Google Scholar 

  • Charvet CJ, Striedter GF (2008) Developmental species differences in brain cell cycle rates between northern bobwhite quail (Colinus virginianus) and parakeets (Melopsittacus undulatus): implications for mosaic brain evolution. Brain Behav Evol 72:295–306

    Google Scholar 

  • Charvet CJ, Striedter GF (2011) Developmental modes and developmental mechanisms can channel brain evolution. Front Neuroanat 5:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Charvet CJ, Striedter GF, Finlay BL (2011) Evo-devo and brain scaling: candidate developmental mechanisms for variation and constancy in vertebrate brain evolution. Brain Behav Evol 78:248–257

    Article  PubMed  PubMed Central  Google Scholar 

  • Charvet CJ, Cahalane DJ, Finlay BL (2015) Systematic, cross-cortex variation in neuron numbers in rodents and primates. Cereb Cortex 25:147–160

    Article  PubMed  Google Scholar 

  • Charvet CJ, Reep RL, Finlay BL (2016) Evolution of cytoarchitectural landscapes in the mammalian isocortex: Sirenians (Trichechus manatus) in comparison with other mammals. J Comp Neurol 524:772–782

    Article  PubMed  Google Scholar 

  • Clancy B, Darlington RB, Finlay BL (2001) Translating developmental time across mammalian species. Neuroscience 105:7–17

    Article  CAS  PubMed  Google Scholar 

  • Deacon TW (1990) Rethinking mammalian brain evolution. Am Zool 30:629–705

    Article  Google Scholar 

  • DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316

    Article  PubMed  Google Scholar 

  • Dehay C, Kennedy H, Kosik KS (2015) The outer subventricular zone and primate-specific cortical complexification. Neuron 85:683–694

    Article  CAS  PubMed  Google Scholar 

  • Diamond IT, Jones EG, Powell TP (1968) The association connections of the auditory cortex of the cat. Brain Res 11:560–579

    Article  CAS  PubMed  Google Scholar 

  • Ding YC, Chi HC, Grady DL et al (2002) Evidence of positive selection acting at the human dopamine receptor D4 gene locus. Proc Natl Acad Sci U S A 99:309–314

    Article  CAS  PubMed  Google Scholar 

  • Dyer MA, Martins R, da Silva Filho M et al (2009) Developmental sources of conservation and variation in the evolution of the primate eye. Proc Natl Acad Sci U S A 106:8963–8968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebstein RP, Novick O, Umansky R et al (1996) Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of novelty seeking. Nat Genet 12:78–80

    Article  CAS  PubMed  Google Scholar 

  • Finlay BL (2008) The developing and evolving retina: using time to organize form. Brain Res 1192:5–16

    Article  CAS  PubMed  Google Scholar 

  • Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584

    Article  CAS  PubMed  Google Scholar 

  • Finlay BL, Hersman MN, Darlington RB (1998) Patterns of vertebrate neurogenesis and the paths of vertebrate evolution. Brain Behav Evol 52:232–242

    Article  CAS  PubMed  Google Scholar 

  • Fujita S, Shimada M, Nakamura T (1966) H3-Thymidine autoradiographic studies on the cell proliferation and differentiation in the external and internal granular layers of the mouse cerebellum. J Comp Neurol 128:191–208

    Article  CAS  PubMed  Google Scholar 

  • García-Cabezas MÁ, Barbas H (2014) Area 4 has layer IV in adult primates. Eur J Neurosci 39:1824–1834

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilbert CD, Kelly JP (1975) The projections of cells in different layers of the cat’s visual cortex. J Comp Neurol 163:81–105

    Article  CAS  PubMed  Google Scholar 

  • Goffinet AM, Daumerie CH, Langerwerf B, Pieau C (1986) Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J Comp Neurol 243:106–116

    Article  CAS  PubMed  Google Scholar 

  • Gona AG (1976) Autoradiographic studies of cerebellar histogenesis in the bullfrog tadpole during metamorphosis: the external granular layer. J Comp Neurol 165:77–87

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Kabelik D, Kelly AM et al (2009) Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proc Natl Acad Sci U S A 106:8737–8742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey RJ, Napper RMA (1988) Quantitative study of granule and Purkinje cells in the cerebellar cortex of the rat. J Comp Neurol 274:151–157

    Article  CAS  PubMed  Google Scholar 

  • Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL et al (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489:391–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc Biol Sci 274:453–464

    Article  PubMed  Google Scholar 

  • Herculano-Houzel S (2012) Neuronal scaling rules for primate brains: the primate advantage. Prog Brain Res 195:325–340

    Article  PubMed  Google Scholar 

  • Hof PR, Nimchinsky EA, Morrison JH (1995) Neurochemical phenotype of corticocortical connections in the macaque monkey: quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. J Comp Neurol 362:109–133

    Article  CAS  PubMed  Google Scholar 

  • Hofman MA (1985) Neuronal correlates of corticalization in mammals: a theory. J Theor Biol 112:77–95

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Gammon SJ, Dieterle M et al (2014) Dramatic increases in number of cerebellar granule-cell-Purkinje-cell synapses across several mammals. Mamm Biol Zeitschrift für Säugetierkunde 79:163–169

    Article  Google Scholar 

  • Kaas JH (1989) Why does the brain have so many visual areas? J Cogn Neurosci 1:121–135

    Article  CAS  PubMed  Google Scholar 

  • Kawamura (1973a) Corticocortical fiber connections of the cat cerebrum. III. The occipital region. Brain Res 51:41–60

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K (1973b) Corticocortical fiber connections of the cat cerebrum. I. The temporal region. Brain Res 51:1–21

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K (1973c) Corticocortical fiber connections of the cat cerebrum. II. The parietal region. Brain Res 51:23–40

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Otani K (1970) Corticocortical fiber connections in the cat cerebrum: the frontal region. J Comp Neurol 139:423–448

    Article  CAS  PubMed  Google Scholar 

  • Markov NT, Vezoli J, Chameau P, Falchier A, Quilodran R, Huissoud C, Lamy C, Misery P, Giroud P, Ullman S, Barone P, Dehay C, Knoblauch K, Kennedy H (2014) Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J Comp Neurol 522:225–259

    Article  PubMed  Google Scholar 

  • Marotte LR, Sheng X-M (2000) Neurogenesis and identification of developing layers in the visual cortex of the wallaby (Macropus eugenii). J Comp Neurol 416:131–142

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Cerdeño V, Cunningham CL, Camacho J et al (2012) Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS One 7:e30178

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller JA, Ding SL, Sunkin SM et al (2014) Transcriptional landscape of the prenatal human brain. Nature 508:199–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nudo RJ, Masterton RB (1990) Descending pathways to the spinal cord, III: sites of origin of the corticospinal tract. J Comp Neurol 296:559–583

    Article  CAS  PubMed  Google Scholar 

  • Nudo RJ, Sutherland DP, Masterton RB (1995) Variation and evolution of mammalian corticospinal somata with special reference to primates. J Comp Neurol 358:181–205

    Article  CAS  PubMed  Google Scholar 

  • O’Connell LA, Hofmann HA (2011) Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 32:320–335

    Article  PubMed  Google Scholar 

  • Paula-Barbosa MM, Feyo PB, Sousa-Pinto A (1975) The association connexions of the suprasylvian fringe (SF) and other areas of the cat auditory cortex. Exp Brain Res 23:535–554

    Article  CAS  PubMed  Google Scholar 

  • Poldrack RA, Farah MJ (2015) Progress and challenges in probing the human brain. Nature 526:371–379

    Article  CAS  PubMed  Google Scholar 

  • Polleux F, Dehay C, Kennedy H (1997) The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J Comp Neurol 385:95–116

    Article  CAS  PubMed  Google Scholar 

  • Ponti G, Peretto P, Bonfanti L (2006) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294:168–180

    Article  CAS  PubMed  Google Scholar 

  • Ponti G, Peretto P, Bonfanti L (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS One 3:e2366

    Article  PubMed  PubMed Central  Google Scholar 

  • Puelles L, Ferran JL (2012) Concept of neural genoarchitecture and its genomic fundament. Front Neuroanat 6:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Puelles L, Rubenstein JL (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469–476

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425–427

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (2002) Pre and post-development of neurogenesis in primates. Clin Neurosci Res 2:29–32

    Article  CAS  Google Scholar 

  • Rakic P (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 13:541–549

    Article  PubMed  Google Scholar 

  • Rakic P, Sidman RL (1970) Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 139:473–500

    Article  CAS  PubMed  Google Scholar 

  • Reep RL, Finlay BL, Darlington RB (2007) The limbic system in mammalian brain evolution. Brain Behav Evol 70:57–70

    Article  CAS  PubMed  Google Scholar 

  • Reyes LD, Stimpson CD, Gupta K, Raghanti MA, Hof PR, Reep RL, Sherwood CC (2015) Neuron types in the presumptive primary somatosensory cortex of the florida manatee (Trichechus manatus latirostris). Brain Behav Evol 86:210–231

    Article  PubMed  Google Scholar 

  • Rowell JJ, Ragsdale CW (2012) BrdU birth dating can produce errors in cell fate specification in chick brain development. J Histochem Cytochem 60:801–810

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowell JJ, Mallik AK, Dugas-Ford J, Ragsdale CW (2010) Molecular analysis of neocortical layer structure in the ferret. J Comp Neurol 518:3272–3289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanderson KJ, Weller WL (1990) Gradients of neurogenesis in possum neocortex. Brain Res Dev 55:269–274

    Article  CAS  Google Scholar 

  • Schmahmann JD, Pandya D (2009) Fiber pathways of the brain. OUP, Oxford

    Google Scholar 

  • Smart IH (1972) Proliferative characteristics of the ependymal layer during the early development of the spinal cord in the mouse. J Anat 111:365–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53

    Article  PubMed  PubMed Central  Google Scholar 

  • Sporns O, Zwi JD (2004) The small world of the cerebral cortex. Neuroinformatics 2:145–162

    Article  PubMed  Google Scholar 

  • Stamatakis A, Barbas H, Dermon CR (2004) Late granule cell genesis in quail cerebellum. J Comp Neurol 474:173–189

    Article  PubMed  Google Scholar 

  • Striedter GF, Keefer BP (2000) Cell migration and aggregation in the developing telencephalon: pulse-labeling chick embryos with bromodeoxyuridine. J Neurosci 20:8021–8030

    Google Scholar 

  • Striedter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Takahashi E, Dai G, Wang R (2010) Development of cerebral fiber pathways in cats revealed by diffusion spectrum imaging. NeuroImage 49:1231–1240

    Article  PubMed  Google Scholar 

  • Takahashi E, Dai G, Rosen GD et al (2011) Developing neocortex organization and connectivity in cats revealed by direct correlation of diffusion tractography and histology. Cereb Cortex 21:200–211

    Article  PubMed  Google Scholar 

  • Takahashi E, Folkerth RD, Galaburda AM, Grant PE (2012) Emerging cerebral connectivity in the human fetal brain: an MR tractography study. Cereb Cortex 22:455–464

    Article  PubMed  Google Scholar 

  • Tsai HM, Garber BB, Larramendi LMH (1981) 3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ. J Comp Neurol 198:275–292

    Article  CAS  PubMed  Google Scholar 

  • Uray NJ, Gona AG, Hauser KF (1987) Autoradiographic studies of cerebellar histogenesis in the premetamorphic bullfrog tadpole: I. Generation of the external granular layer. J Comp Neurol 266:234–246

    Article  CAS  PubMed  Google Scholar 

  • Vallender EJ (2011) Comparative genetic approaches to the evolution of human brain and behavior. Am J Hum Biol 23:53–64

    Article  PubMed  PubMed Central  Google Scholar 

  • Vallender EJ (2012) Genetic correlates of the evolving primate brain. Prog Brain Res 195:27–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Cogn Sci 2:307–313

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Ding YC et al (2004) The genetic architecture of selection at the human dopamine receptor D4 (DRD4) gene locus. Am J Hum Genet 74:931–944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wedeen VJ, Rosene DL, Wang R et al (2012) The geometric structure of the brain fiber pathways. Science 335:1628–1634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson M, Hume R, Strange R, Bell JE (1990) Glial and neuronal differentiation in the human fetal brain 9–23 weeks of gestation. Neuropathol Appl Neurobiol 16:193–204

    Article  CAS  PubMed  Google Scholar 

  • Workman AD, Charvet CJ, Clancy B et al (2013) Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci 33:7368–7383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Mirabeau O, Bureau C et al (2013) Evolution of dopamine receptor genes of the D1 class in vertebrates. Mol Biol Evol 30:833–843

    Article  CAS  PubMed  Google Scholar 

  • Yamawaki N, Borges K, Suter BA, Harris KD, Shepherd GM (2014) A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity. eLife 3:e05422

    PubMed  PubMed Central  Google Scholar 

  • Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054

    Article  CAS  PubMed  Google Scholar 

  • Yurkewicz L, Lauder JM, Marchi M, Giacobini E (1981) 3H-Thymidine long survival autoradiography as a method for dating the time of neuronal origin in the chick embryo: the locus coeruleus and cerebellar Purkinje cells. J Comp Neurol 203:257–267

    Article  CAS  PubMed  Google Scholar 

  • Zeng H, Shen EH, Hohmann JG et al (2012) Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 149:483–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the James S. McDonnell Foundation Grant 22002078 (C. C. S.), the Eunice Shriver Kennedy NICHD R01HD078561 and R21HD069001 (E. T.), as well as a DAAD grant (C. J. C). Images of Nissl-stained sections of primary visual cortex of the macaque and rat as well as the cerebellum of the macaque shown in Figs. 4.4 and 4.5 were obtained by taking screenshots from brainmaps.org. We also used gene expression data from the BrainSpan: Atlas of the Developing Human Brain, funded by ARRA Awards 1RC2MH089921-01, 1RC2MH090047-01, and 1RC2MH089929-01. These data are available from http://developinghumanbrain.org

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Charvet, C.J., Sherwood, C.C., Takahashi, E. (2017). Developmental Sequences Predict Increased Connectivity in Brain Evolution: A Comparative Analysis of Developmental Timing, Gene Expression, Neuron Numbers, and Diffusion MR Tractography. In: Watanabe, S., Hofman, M., Shimizu, T. (eds) Evolution of the Brain, Cognition, and Emotion in Vertebrates. Brain Science. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56559-8_4

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