The evolution of nervous system centralization
Open accessAbstract
It is yet unknown when and in what form the central nervous system in Bilateria first came into place and how it further evolved in the different bilaterian phyla. To find out, a series of recent molecular studies have compared neurodevelopment in slow-evolving deuterostome and protostome invertebrates, such as the enteropneust hemichordate Saccoglossus and the polychaete annelid Platynereis. These studies focus on the spatially different activation and, when accessible, function of genes that set up the molecular anatomy of the neuroectoderm and specify neuron types that emerge from distinct molecular coordinates. Complex similarities are detected, which reveal aspects of neurodevelopment that most likely occurred already in a similar manner in the last common ancestor of the bilaterians, Urbilateria. This way, different aspects of the molecular architecture of the urbilaterian nervous system are reconstructed and yield insight into the degree of centralization that was in place in the bilaterian ancestors.
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.
Integrity signals
Registry
Cites
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.
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?
These neurons can subsequently diverge to form sister cell types.
“These neurons can subsequently diverge to form sister cell types [22].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [22]
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
Ghrelin: Structure and Function
Kojima, M., & Kangawa, K. (2005) · Physiological Reviews · doi:10.1152/physrev.00012.2004 · Cited by 2,810 · see citing works
The origin of pattern and polarity in the Drosophila embryo
Johnston, D. S., & Nüsslein‐Volhard, C. (1992) · Cell · doi:10.1016/0092-8674(92)90466-p · Cited by 1,337 · see citing works
Pax6 Controls Progenitor Cell Identity and Neuronal Fate in Response to Graded Shh Signaling
Ericson, J., Rashbass, P., Schedl, A., Brenner‐Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., & Briscoe, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80323-2 · Cited by 1,044 · see citing works
FORMATION AND FUNCTION OF SPEMANN'S ORGANIZER
Harland, R., & Gerhart, J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.611 · Cited by 839 · see citing works
Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling
Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T., Rubenstein, J., & Ericson, J. (1999) · Nature · doi:10.1038/19315 · Cited by 807 · see citing works
A common plan for dorsoventral patterning in Bilateria
De Robertis, E. M., & Sasai, Y. (1996) · Nature · doi:10.1038/380037a0 · Cited by 780 · see citing works
Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus
Sasai, Y., Lu, B., Steinbeißer, H., & Robertis, E. M. D. (1995) · Nature · doi:10.1038/376333a0 · Cited by 717 · see citing works
The zootype and the phylotypic stage
Slack, J. M. W., Holland, P. W. H., & Graham, C. F. (1993) · Nature · doi:10.1038/361490a0 · Cited by 699 · see citing works
Longitudinal organization of the anterior neural plate and neural tube
Shimamura, K., Hartigan-O’Connor, D. J., Martı́nez, S., Puelles, L., & Rubenstein, J. L. R. (1995) · Development · doi:10.1242/dev.121.12.3923 · Cited by 657 · see citing works
REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE
Rubenstein, J. L. R., Shimamura, K., Martı́nez, S., & Puelles, L. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.445 · Cited by 546 · see citing works
Anteroposterior patterning in hemichordates and the origins of the chordate nervous system
Lowe, C. J., Wu, M., Salic, A., Evans, L., Lander, E., Stange-Thomann, N., Gruber, C. E., Gerhart, J., & Kirschner, M. (2003) · Cell · doi:10.1016/s0092-8674(03)00469-0 · Cited by 531 · see citing works
Denes, A. S., Jékely, G., Steinmetz, P. R. H., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D. E. K., Balavoine, G., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.02.040 · Cited by 480 · see citing works
Self-citationCiliary photoreceptors with a vertebrate-type opsin in an invertebrate brain
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W., & Wittbrodt, J. (2004) · Science · doi:10.1126/science.1099955 · Cited by 458 · see citing works
Self-citationSchmidt, B. J., & Jordan, L. M. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00402-0 · Cited by 425 · see citing works
Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution
Lowe, C. J., Terasaki, M., Wu, M., Freeman, R. M., Runft, L., Kwan, K., Haigo, S., Aronowicz, J., Lander, E., Gruber, C., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040291 · Cited by 385 · see citing works
Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.04.041 · Cited by 384 · see citing works
Self-citationInversion of dorsoventral axis?
Arendt, D., & Nübler‐Jung, K. (1994) · Nature · doi:10.1038/371026a0 · Cited by 334 · see citing works
Self-citationHuman BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo.
Padgett, R. W., Wozney, J. M., & Gelbart, W. M. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.7.2905 · Cited by 285 · see citing works
Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain
Mastick, G. S., Davis, N. M., Andrews, G. L., & Easter, S. S. (1997) · Development · doi:10.1242/dev.124.10.1985 · Cited by 269 · see citing works
Comparison of early nerve cord development in insects and vertebrates
Arendt, D., & Nübler-Jung, K. (1999) · Development · doi:10.1242/dev.126.11.2309 · Cited by 258 · see citing works
Self-citationVertebrate-Type Intron-Rich Genes in the Marine Annelid <i>Platynereis dumerilii</i>
Raible, F., Tessmar-Raible, K., Osoegawa, K., Wincker, P., Jubin, C., Balavoine, G., Ferrier, D., Benes, V., de Jong, P., Weissenbach, J., et al. (2005) · Science · doi:10.1126/science.1119089 · Cited by 257 · see citing works
Self-citationAxial patterning in cephalochordates and the evolution of the organizer
Yu, J., Satou, Y., Holland, N. D., Shin‐I, T., Kohara, Y., Satoh, N., Bronner-Fraser, M. E., & Holland, L. Z. (2007) · Nature · doi:10.1038/nature05472 · Cited by 256 · see citing works
Molecular anatomy of placode development in Xenopus laevis
Schlosser, G., & Ahrens, K. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.013 · Cited by 252 · see citing works
Early central nervous system evolution: an era of skin brains?
Holland, N. D. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1175 · Cited by 250 · see citing works
Molecular evidence for deep evolutionary roots of bilaterality in animal development
Matus, D. Q., Pang, K., Marlow, H. Q., Dunn, C. W., Thomsen, G. H., & Martindale, M. Q. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601257103 · Cited by 227 · see citing works
Molecular markers for identified neuroblasts in the developing brain ofDrosophila
Urbach, R., & Technau, G. M. (2003) · Development · doi:10.1242/dev.00533 · Cited by 224 · see citing works
Proposal of a model of mammalian neural induction
Levine, A. J., & Brivanlou, A. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.05.036 · Cited by 195 · see citing works
Mineta, K., Nakazawa, M., Cebrià, F., Ikeo, K., Agata, K., & Gojobori, T. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1332513100 · Cited by 189 · see citing works
Formation of the BMP Activity Gradient in the Drosophila Embryo
Mizutani, C. M., Nie, Q. H., Wan, F. Y. M., Zhang, Y.-T., Vilmos, P., Sousa‐Neves, R., Bier, E., Marsh, J., & Lander, A. D. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.04.009 · Cited by 185 · see citing works
Rentzsch, F., Anton, R., Saina, M., Hammerschmidt, M., Holstein, T. W., & Technau, U. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.06.003 · Cited by 170 · see citing works
Vnd/nkx, ind/gsh, and msh/msx: conserved regulators of dorsoventral neural patterning?
Cornell, R. A., & Ohlen, T. L. V. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00049-5 · Cited by 161 · see citing works
Otx dose-dependent integrated control of antero-posterior and dorso-ventral patterning of midbrain
Puelles, E., Acampora, D., Lacroix, E., Signore, M., Annino, A., Tuorto, F., Filosa, S., Corte, G., Wurst, W., Ang, S., et al. (2003) · Nature Neuroscience · doi:10.1038/nn1037 · Cited by 157 · see citing works
Lichtneckert, R., & Reichert, H. (2005) · Heredity · doi:10.1038/sj.hdy.6800664 · Cited by 153 · see citing works
Common ground plans in early brain development in mice and flies
Arendt, D., & Nübler‐Jung, K. (1996) · BioEssays · doi:10.1002/bies.950180314 · Cited by 142 · see citing works
Self-citationCentral Neural Circuitry in the Jellyfish <i>Aglantha</i>
Mackie, G. O. (2004) · Neurosignals · doi:10.1159/000076155 · Cited by 128 · see citing works
Role ofPax3/7in the tectum regionalization
Matsunaga, E., Araki, I., & Nakamura, H. (2001) · Development · doi:10.1242/dev.128.20.4069 · Cited by 123 · see citing works
The murine homeobox gene Msx-3 shows highly restricted expression in the developing neural tube
Shimeld, S. M., McKay, I. J., & Sharpe, P. T. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(96)00505-9 · Cited by 119 · see citing works
Cheesman, S. E., Layden, M. J., Ohlen, T. L. V., Doe, C. Q., & Eisen, J. S. (2004) · Development · doi:10.1242/dev.01397 · Cited by 119 · see citing works
Mizutani, C. M., Meyer, N. P., Roelink, H., & Bier, E. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040313 · Cited by 119 · see citing works
Pattyn, A., Vallstedt, A., Dias, J. M., Sander, M., & Ericson, J. (2003) · Development · doi:10.1242/dev.00641 · Cited by 112 · see citing works
Origins of anteroposterior patterning and Hox gene regulation during chordate evolution
Schilling, T. F., & Kinght, R. D. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0918 · Cited by 111 · see citing works
Urbach, R., & Technau, G. M. (2003) · Development · doi:10.1242/dev.00532 · Cited by 110 · see citing works
Pax3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy
Davis, G. K., D’Alessio, J. A., & Patel, N. H. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.06.014 · Cited by 107 · see citing works
Miljkovic‐Licina, M., Gauchat, D., & Galliot, B. (2004) · Biosystems · doi:10.1016/j.biosystems.2004.05.030 · Cited by 93 · see citing works
Westfall, J. A., Elliott, C. F., & Carlin, R. W. (2002) · Journal of Morphology · doi:10.1002/jmor.1075 · Cited by 83 · see citing works
Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain
Arendt, D., Tessmar‐Raible, K., Snyman, H., Dorresteijn, A. W. C., & Wittbrodt, J. (2005) · e-Neuroforum · doi:10.1515/nf-2005-0106 · Cited by 82 · see citing works
Self-citationMotor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms.
Thor, S., & Thomas, J. B. (2002) · Current Opinion in Genetics and Development · doi:10.1016/s0959-437x(02)00340-4 · Cited by 77 · see citing works
Takacs, C. M., Amore, G., Oliveri, P., Poustka, A. J., Wang, D., Burke, R. D., & Peterson, K. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.023 · Cited by 75 · see citing works
Zaffran, S., Das, G., & Frasch, M. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00298-7 · Cited by 62 · see citing works
Gene expression patterns in primary neuronal clusters of the Drosophila embryonic brain
Sprecher, S. G., Reichert, H., & Hartenstein, V. (2007) · Gene Expression Patterns · doi:10.1016/j.modgep.2007.01.004 · Cited by 58 · see citing works
Rusten, T. E., Cantera, R., Kafatos, F. C., & Barrio, R. (2002) · Development · doi:10.1242/dev.129.15.3575 · Cited by 32 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Bullock T.H, Horridge G.A. Structure and function in the nervous system of invertebrates. Freeman; San Francisco, CA; London, UK: 1965. [Google Scholar]
Cited by
Sorted by citations
Allostasis: A brain-centered, predictive mode of physiological regulation
Schulkin, J., & Sterling, P. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.07.010 · Cited by 265 · see citing works
Cnidarians and the evolutionary origin of the nervous system
Watanabe, H., Fujisawa, T., & Holstein, T. W. (2009) · Development, Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01103.x · Cited by 206 · see citing works
The evolution of associative learning: A factor in the Cambrian explosion
Ginsburg, S., & Jablonka, E. (2010) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2010.06.017 · Cited by 184 · see citing works
Independent origins of neurons and synapses: insights from ctenophores
Moroz, L. L., & Kohn, A. B. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0041 · Cited by 171 · see citing works
Origins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168 · see citing works
The Evolution of Early Neurogenesis
Hartenstein, V., & Stollewerk, A. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.02.004 · Cited by 161 · see citing works
Evolution of centralized nervous systems: Two schools of evolutionary thought
Northcutt, R. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201889109 · Cited by 141 · see citing works
BMPs and Chordin regulate patterning of the directive axis in a sea anemone
Saina, M., Genikhovich, G., Renfer, E., & Technau, U. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900151106 · Cited by 138 · see citing works
Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis
Watanabe, H., Kuhn, A., Fushiki, M., Agata, K., Özbek, S., Fujisawa, T., & Holstein, T. W. (2014) · Nature Communications · doi:10.1038/ncomms6536 · Cited by 79 · see citing works
Convergence of ion channel genome content in early animal evolution
Liebeskind, B. J., Hillis, D. M., & Zakon, H. H. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501195112 · Cited by 76 · see citing works
Yuan, Z., Shao, X., Miao, Z., Zhao, B., Zheng, Z., & Zhang, J. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.05.011 · Cited by 64 · see citing works
The genealogy of genealogy of neurons
Moroz, L. L. (2014) · Communicative & Integrative Biology · doi:10.4161/19420889.2014.993269 · Cited by 59 · see citing works
Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria)
Piraino, S., Zega, G., Di Benedetto, C., Leone, A., Dell'Anna, A., Pennati, R., Candia Carnevali, D., Schmid, V., & Reichert, H. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22614 · Cited by 56 · see citing works
Evolutionary development of neural systems in vertebrates and beyond
O’Connell, L. A. (2013) · Journal of Neurogenetics · doi:10.3109/01677063.2013.789511 · Cited by 17 · see citing works
- Authors
- Arendt, D., Denes, A. S., Jékely, G., & Tessmar-Raible, K.
- Affiliations
- European Molecular Biology Laboratory (DE)
- Developmental Biology Unit, European Molecular Biology LaboratoryHeidelberg 69117, Germany
- Venue
- Philosophical Transactions of the Royal Society B Biological Sciences
- Publisher
- The Royal Society
- Published
- 2008-01-11
- Volume
- 363
- Issue
- 1496
- Pages
- 1523-1528
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC2614231
- OpenAlex
- W2155253806
- Cited by
- 206
- References
- 51
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 4 · 2023: 6 · 2022: 9 · 2021: 8 · 2020: 8 · 2019: 10 · 2018: 9 · 2017: 18 · 2016: 11 · 2015: 22 · 2014: 13 · 2013: 11 · 2012: 12
- FWCI
- 1.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Boehringer Ingelheim Stiftung
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- nervous system evolution, centralization, brain development, Urbilateria, Platynereis, hemichordates, Polychaeta, neuroectoderm, deuterostomes, protostomes
- MeSH terms
- Animals, Central Nervous System, Biological Evolution, Invertebrates, Models, Neurological, Vertebrates, Gene Expression Regulation, Developmental, Evolution, Molecular, Body Patterning
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
