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Scalable architecture in mammalian brains

Abstract

Comparison of mammalian brain parts has often focused on differences in absolute size1,2,3, revealing only a general tendency for all parts to grow together2. Attempts to find size-independent effects using body weight as a reference variable1 obscure size relationships owing to independent variation of body size4 and give phylogenies of questionable significance5. Here we use the brain itself as a size reference to define the cerebrotype, a species-by-species measure of brain composition. With this measure, across many mammalian taxa the cerebellum occupies a constant fraction of the total brain volume (0.13 ± 0.02), arguing against the hypothesis that the cerebellum acts as a computational engine principally serving the neocortex3. Mammalian taxa can be well separated by cerebrotype, thus allowing the use of quantitative neuroanatomical data to test evolutionary relationships. Primate cerebrotypes have progressively shifted and neocortical volume fractions have become successively larger in lemurs and lorises, New World monkeys, Old World monkeys, and hominoids, lending support to the idea that primate brain architecture has been driven by directed selection pressure4. At the same time, absolute brain size can vary over 100-fold within a taxon, while maintaining a relatively uniform cerebrotype. Brains therefore constitute a scalable architecture.

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Figure 1: Analysis of volumetric data from mammalian brains.
Figure 2: Constancy of cerebellar volume fraction across mammalian taxa.
Figure 3: Clustering of cerebrotypes by taxon.
Figure 4: Clustering of cerebrotypes within taxa.
Figure 5: Evolutionary trends in brain architecture.

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Acknowledgements

We thank J. M. Allman and M. J. Berry for discussions, R. Kasthuri for research assistance, and T. A. Barney for secretarial assistance. D.A.C. is in the Princeton University Program in Biophysics. S.S.-H.W. is supported by the Alfred P. Sloan Foundation.

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Correspondence to Samuel S.-H. Wang.

Supplementary information

Figure a (GIF 10.6 KB)

Figure b (GIF 7.85 KB)

Figure c (GIF 8.35 KB)

Primate key

  • sp32 Cheirogaleus major

  • sp33 Cheirogaleus medius

  • sp34 Microcebus murinus

  • sp35 Lepilemur ruficaudatus

  • sp36 Lemur fulvus

  • sp37 Lemur variegatus

  • sp38 Avahi l. laniger

  • sp39 Avahi l. occidentalis

  • sp40 Propithecus verreauxi

  • sp41 Indri indri

  • sp42 Daubentonia madagasc.

  • sp43 Loris tardigradus

  • sp44 Nycticebus coucang

  • sp45 Perodicticus potto

  • sp46 Galago crassicaudatus

  • sp47 Galago demidoff

  • sp48 Galago senegalensis

  • sp49 Tarsius sp.

  • sp50 Callithrix jacchus

  • sp51 Cebuella pygmaea

  • sp52 Saguinus oedipus

  • sp53 Saguinus tamarin

  • sp54 Callimico goeldii

  • sp55 Aotus trivirgatus

  • sp56 Pithecia monachus

  • sp57 Alouatta sp.

  • sp58 Ateles geoffroyi

  • sp59 Lagothrix lagotricha

  • sp60 Cebus sp.

  • sp61 Saimiri sciureus

  • sp62 Macaca mulatta

  • sp63 Cercocebus albigena

  • sp64 Papio anubis

  • sp65 Cercopithecus mitis

  • sp66 Cercopithecus ascan.

  • sp67 Cercopithecus talap.

  • sp68 Erythrocebus patas

  • sp69 Pygathrix nemaeus

  • sp70 Nasalis larvatus

  • sp71 Colobus badius

  • sp72 Hylobates lar

  • sp73 Pan troglodytes

  • sp74 Gorilla gorilla

  • sp75 Homo sapiens sapiens

  • sp76 Pongo pygmaeus

Clark_data (TXT 22.4 KB)

What's what in 'Clark_data.txt': The file is tab-delimited. Raw volume data from Stephan et al. (1981). All volumes given are in mm^3 unless otherwise noted.

  • Rows indicate regions as follows:

  • 1 body weight in grams

  • 2 brain weight in mg

  • 3 ventricles

  • 4 meninges, hypophysis, nerves, etc.

  • 5 total brain

  • 6 medulla oblongata

  • 7 cerebellum

  • 8 mesencephalon

  • 9 diencephalon

  • 10 telencephalon

  • 11 bulbus olfactorius

  • 12 bulbus olfactorius accessorius

  • 13 lobus piriformis

  • 14 septum

  • 15 striatum

  • 16 schizocortex

  • 17 hippocampus

  • 18 neocortex

  • Columns are species as follows (The ordering is the same as in Stephan et al. Callicebus moloch is excluded because of a checksum error.):

  • The ordering is the same as in Stephan et al.

  • Callicebus moloch is excluded because of a checksum error.

  • 1 Solenodon paradoxus

  • 2 Tenrec ecaudatus

  • 3 Setifer setosus

  • 4 Hemicentetes semispin.

  • 5 Echinops telfairi

  • 6 Oryzorictes talpoides

  • 7 Microgale cowani

  • 8 Limnogale mergulus

  • 9 Nesogale dobsoni

  • 10 Nesogale talazaci

  • 11 Micropotamogale lamottei

  • 12 Potamogale velox

  • 13 Chlorotalpa stuhlmanni

  • 14 Chrysochloris asiatica

  • 15 Aethechinus algirus

  • 16 Erinaceus europaeus

  • 17 Hemiechinus auritus

  • 18 Elephantulus fuscipes

  • 19 Rhynchocyon stuhlmanni

  • 20 Sorex minutus

  • 21 Sorex araneus

  • 22 Neomys fodiens

  • 23 Crocidura occidentalis

  • 24 Crocidura russula

  • 25 Suncus murinus

  • 26 Talpa europaea

  • 27 Desmana moschata

  • 28 Galemys pyrenaicus

  • 29 Tupaia glis

  • 30 Tupaia minor

  • 31 Urogale everetti

  • 32 Cheirogaleus major

  • 33 Cheirogaleus medius

  • 34 Microcebus murinus

  • 35 Lepilemur ruficaudatus

  • 36 Lemur fulvus

  • 37 Lemur variegatus

  • 38 Avahi l. laniger

  • 39 Avahi l. occidentalis

  • 40 Propithecus verreauxi

  • 41 Indri indri

  • 42 Daubentonia madagasc.

  • 43 Loris tardigradus

  • 44 Nycticebus coucang

  • 45 Perodicticus potto

  • 46 Galago crassicaudatus

  • 47 Galago demidoff

  • 48 Galago senegalensis

  • 49 Tarsius sp.

  • 50 Callithrix jacchus

  • 51 Cebuella pygmaea

  • 52 Saguinus oedipus

  • 53 Saguinus tamarin

  • 54 Callimico goeldii

  • 55 Aotus trivirgatus

  • 56 Pithecia monachus

  • 57 Alouatta sp.

  • 58 Ateles geoffroyi

  • 59 Lagothrix lagotricha

  • 60 Cebus sp.

  • 61 Saimiri sciureus

  • 62 Macaca mulatta

  • 63 Cercocebus albigena

  • 64 Papio anubis

  • 65 Cercopithecus mitis

  • 66 Cercopithecus ascan.

  • 67 Cercopithecus talap.

  • 68 Erythrocebus patas

  • 69 Pygathrix nemaeus

  • 70 Nasalis larvatus

  • 71 Colobus badius

  • 72 Hylobates lar

  • 73 Pan troglodytes

  • 74 Gorilla gorilla

  • 75 Homo sapiens sapiens

Clark_tables (XLS 25.0 KB)

Clark_data (PDF 551 kb)

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Clark, D., Mitra, P. & Wang, SH. Scalable architecture in mammalian brains. Nature 411, 189–193 (2001). https://doi.org/10.1038/35075564

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  • DOI: https://doi.org/10.1038/35075564

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