Research Article

Birds have primate-like numbers of neurons in the forebrain

Seweryn Olkowicz, Martin Kocourek, Radek K. Lučan, Michal Porteš, W. Tecumseh Fitch, Suzana Herculano-Houzel, and Pavel Němec
PNAS June 28, 2016 113 (26) 7255-7260; first published June 13, 2016; https://doi.org/10.1073/pnas.1517131113

  1. Edited by Dale Purves, Duke University, Durham, NC, and approved May 6, 2016 (received for review August 27, 2015)

  1. Fig. S1.
    Fig. S1.

    Phylogenetic relationships among the 28 species examined. The tree was constructed using birdtree.org/; its topology follows recent studies (46–49). Note that songbirds and parrots are sister groups and together with the distantly related barn owl belong to the clade core landbirds (Telluraves); the pigeon represents the Columbea, a basal clade of the Neoaves; the red junglefowl represents the Galloanseres, a sister group of Neoaves and the most basal clade of Neognathae; and the emu represents Paleognathae (tinamous and flightless ostriches), the most basal clade of extant birds (48). Also note that all passerine birds examined were vocal learners belonging to the clade Oscines.

  2. Fig. S2.
    Fig. S2.

    Brain dissection and labeling of neurons and nonneuronal cells. (A and B) Brain of the raven before and after the dissection. (A) Ventral side of the brain showing approximate lines of dissection of the brainstem and tectum. (B) Brain dissected into parts used for isotropic fractionation. (C) NeuN-immunolabeled transverse section of the zebra finch brain depicting the line of dissection of the tectum from the rest of the mesencephalon. (D–F) Dissection of the telencephalon into pallium and subpallium. NeuN-immunolabeled transverse sections of the zebra finch brain at rostral (D), intermediate (E), and caudal (F) telencephalic levels. Lines of dissection follow the pallial-subpallial lamina and divide the telencephalon into pallium (dorsal part) and subpallium (ventral part). Coordinates anterior to the Y point are indicated in millimeters at Bottom Left (64). (G–I) High-power micrographs showing a sample of homogenate from the telencephalon of the Eurasian jay; dissociated nuclei stained with DAPI (G) and immunolabeled with NeuN antibody (H), dual-fluorescence merge image (I). Note that neurons are double-labeled, whereas the nonneuronal cells are devoid of anti-NeuN immunoreactivity. [Scale bars: 10 mm (A and B); 1 mm (C and F); 50 µm (I).]

  3. Fig. 1.
    Fig. 1.

    Cellular scaling rules for brains of songbirds and parrots compared with those for mammals. (A) Avian and mammalian brains depicted at the same scale. Numbers under each brain represent brain mass (in grams) and total number of brain neurons (in millions). Notice that brains of songbirds (goldcrest, starling, and rook) and parrots (cockatoo) contain more than twice as many neurons as rodent (mouse and rat) and primate (marmoset and galago) brains of similar size. (Scale bar: 10 mm.) (B) Brain mass plotted as a function of total number of neurons. Note that allometric lines for songbirds (green line) and parrots (red line) do not differ from each other, but they do differ from allometric lines for mammals (for statistics, see SI Results). (C) Brain mass plotted as a function of total number of nonneuronal cells. (D) Brain mass plotted as a function of body mass. (E) Total number of brain neurons plotted as a function of body mass. Allometric lines for the taxa examined are significantly different (for statistics, see SI Results). Each point represents the average values for one species. Data points representing noncorvid songbirds are light green, and data points representing corvid songbirds are dark green. The fitted lines represent reduced major axis (RMA) regressions and are shown only for correlations that are significant [coefficient of determination (r2) ranges between 0.831 and 0.997; P ≤ 0.021 in all cases]. Because nonneuronal scaling rules are very similar across the clades analyzed, the regression lines are omitted in C. Data for mammals are from published reports (for details, see Methods). CL, pigeon (Columba livia); DN, emu (Dromaius novaehollandiae); GG, red junglefowl (Gallus gallus); TA, barn owl (Tyto alba).

  4. Fig. 2.
    Fig. 2.

    Cellular densities in avian brains. (A) Lateral view of the starling brain showing the brain regions analyzed (for details, see SI Methods and Fig. S2). Neuronal (B and C) and nonneuronal cell density (D and E) plotted as a function of brain mass. Data points representing noncorvid songbirds are light green, and data points representing corvid songbirds are dark green. All graphs are plotted using the same y-axis scale for comparison. Note that neuronal density varies greatly among principal brain divisions and decreases significantly with increasing brain mass in all divisions but the telencephalon, whereas nonneuronal cell density is similar across brain divisions and species, but lower in the telencephalon (for statistics, see SI Results). The fitted lines represent RMA regressions and are shown only for correlations that are significant (r2 ranges between 0.410 and 0.962; P ≤ 0.030 in all cases).

  5. Fig. 3.
    Fig. 3.

    Neuronal densities and relative distribution of neurons in birds and mammals. (A–C) Neuronal densities in the pallium (A), cerebellum (B), and rest of the brain (C). Note that neuronal densities are higher in parrots and songbirds than in mammals (for statistics, see SI Results). (D–F) Average proportions of neurons contained in the pallium (D), cerebellum (E), and rest of the brain (F). Note that increasing proportions of brain neurons in the rest of the brain in parrots are attributable specifically to increasing numbers of neurons in the subpallium (Fig. 5). Data points representing noncorvid songbirds are light green, and data points representing corvid songbirds are dark green. The fitted lines represent RMA regressions and are shown only for correlations that are significant (r2 ranges between 0.389 and 0.956; P ≤ 0.033 in all cases). (G) Brains of corvids (jay and raven), parrots (macaw), and primates (monkeys) are drawn at the same scale. Numbers under each brain represent mass of the pallium (in grams) and total numbers of pallial/cortical neurons (in millions). Circular graphs show proportions of neurons contained in the pallium (green), cerebellum (red), and rest of the brain (yellow). Notice that brains of these highly intelligent birds harbor absolute numbers of neurons that are comparable, or even larger than those of primates with much larger brains. (Scale bar: 10 mm.) Data for mammals are from published reports (for details, see Methods). CL, pigeon; DN, emu; GG, red junglefowl; TA, barn owl.

  6. Fig. S3.
    Fig. S3.

    Brain size, morphology, and number of neurons for the avian species examined. Dorsal and lateral views of representative brains are accompanied by information concerning total number of brain neurons (yellow), number of pallial neurons (blue), and brain mass (red). M, million. (Scale bar, 10 mm.)

  7. Fig. S4.
    Fig. S4.

    Brain–body scaling in birds and mammals. (A and B) Taxonomic differences in relative brain size among songbirds (including both Oscines and Suboscines), parrots, primates, and nonprimate mammals. Inset in A corresponds to the magnified view shown in B. Note that allometric lines for these taxonomic groups are significantly different [full-factorial ANCOVA, slopes: F(3,2618) = 78.43, P < 10−6; intercepts: F(3,2618) = 7.44, P < 10−4; post hoc analyses indicate that the regression line for primates has a different slope (P < 0.001 for all pairwise comparisons) and that parrots and songbirds have significantly larger brains for a given body mass than nonprimate mammals (P < 10−6 for both planned comparisons)]. (C) Relative brain size differences among parrots, corvids, and noncorvid songbirds. Note that allometric lines for these taxonomic groups are significantly different [slopes: F(2,996) = 4.24, P = 0.014; intercepts: F(2,996) = 5.99, P = 0.003; post hoc analyses indicate the regression line for songbirds has a different slope (P ≤ 0.045 for both pairwise comparisons) and that parrots have significantly larger brains for a given body mass than corvids (P < 10−6)]. Mean brain mass versus mean body mass for species are plotted; the fitted lines represent reduced major axis regressions. The relationship between brain mass and body mass can be described by the following power functions: songbirds, MBR = 0.087 × MBO0.737, r2 = 0.953; noncorvid songbirds, MBR = 0.096 × MBO0.698, r2 = 0.92; corvids, MBR = 0.097 × MBO0.725, r2 = 0.952; parrots, MBR = 0.123 × MBO0.716, r2 = 0.954; primates, MBR = 0.061 × MBO0.823, r2 = 0.925; nonprimate mammals, MBR = 0.055 × MBO0.730, r2 = 0.977; all values of P < 0.0001. The data on body mass and brain mass were collated from the literature (for references, see Dataset S3); cetaceans were excluded from the dataset.

  8. Fig. S5.
    Fig. S5.

    Quantitative data currently available for the avian and mammalian species examined with the isotropic fractionator. (A–D) Species ranked in descending order from the largest to the smallest body mass (A), brain mass (B), total number of brain neurons (C), and total number of pallial neurons (D). The mean values of these variables are given in brackets. (E) Median ranks for the avian and mammalian clades examined. Data for mammals are from published reports (32–39).

  9. Fig. 4.
    Fig. 4.

    Relative distribution of mass and cells in avian brains. Average percentages of mass (A and B), number of neurons (C and D), and number of nonneuronal cells (E and F) contained in the principal brain divisions relative to the whole brain in each species, plotted against brain mass. Data points representing noncorvid songbirds are light green, and data points representing corvid songbirds are dark green. The fitted lines represent RMA regressions and are shown only for correlations that are significant (r2 ranges between 0.389 and 0.956; P ≤ 0.023 in all cases). Note that both telencephalon mass fraction and proportions of neuronal and nonneuronal cells contained in the telencephalon increase with brain size.

  10. Fig. 5.
    Fig. 5.

    Subpallium in avian telencephalon. (A) Diagram of sagittal section through the zebra finch brain showing relative position and size of the pallium and subpallium. (B and C) Average percentages of mass (B), number of neurons (C) contained in the subpallium relative to the whole telencephalon in each species, plotted against telencephalon mass. (D) Relationship between numbers of subpallial and pallial neurons. Note that, in parrots, the number of neurons in the subpallium increases faster than in the pallium (scaling exponent = 1.19 ± 0.13), whereas an opposite trend is observed in songbirds (scaling exponent = 0.91 ± 0.1). The fitted lines represent RMA regressions and are shown only for correlations that are significant (r2 ranges between 0.379 and 0.981; P ≤ 0.025 in all cases). Songbirds shown in green (data points representing noncorvids are light green, and data points representing corvids are dark green), parrots in red, and other birds in black. CL, pigeon; DN, emu; GG, red junglefowl; TA, barn owl.

  11. Fig. S6.
    Fig. S6.

    Glia/neuron ratios for the avian species examined. Each point represents the average proportion of nonneuronal cells (left axis) and the glia/neuron ratio (right axis) for one species, plotted against the average brain mass for that species. Songbirds are shown in green, parrots in red, and other birds in black. (A) The overall glia/neuron ratio in the brain. Note the higher proportion of nonneuronal cells in all outgroup taxa. (B) Variation in the glia/neuron ratio among the principal brain divisions investigated. Note that nonneuronal cells constitute a minor cellular fraction in the telencephalon of all species except three representatives of basal bird lineages—the emu, the red junglefowl, and the pigeon. Also note the high proportion of nonneuronal cells in the brainstem and the diencephalon.

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Cellular scaling rules for bird brains
Seweryn Olkowicz, Martin Kocourek, Radek K. Lučan, Michal Porteš, W. Tecumseh Fitch, Suzana Herculano-Houzel, Pavel Němec
Proceedings of the National Academy of Sciences Jun 2016, 113 (26) 7255-7260; DOI: 10.1073/pnas.1517131113
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Proceedings of the National Academy of Sciences: 113 (26)
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