INTRODUCTION: Songbirds, especially corvids, and parrots are remarkably intelligent. Their cognitive skills are on par with primates and their brains contain primate-like numbers of neurons concentrated in high densities in the telencephalon. Much less is known about cognition and neuron counts in more basal bird lineages. Here, we focus on brain cellular composition of galliform birds, which have small brains relative to body size and a proportionally small telencephalon and are often perceived as cognitively inferior to most other birds. METHODS: We use the isotropic fractionator to assess quantitatively the numbers and distributions of neurons and nonneuronal cells in 15 species of galliform birds and compare their cellular scaling rules with those of songbirds, parrots, marsupials, insectivores, rodents, and primates. RESULTS: On average, the brains of galliforms contain about half the number of neurons found in parrot and songbird brains of the same mass. Moreover, in contrast to these birds, galliforms resemble mammals in having small telencephalic and dominant cerebellar neuronal fractions. Consequently, galliforms have much smaller absolute numbers of neurons in their forebrains than equivalently sized songbirds and parrots, which may limit their cognitive abilities. However, galliforms have similar neuronal densities and neuron counts in the brain and forebrain as equally sized non-primate mammals. Therefore, it is not surprising that cognitive abilities of galliforms are on par with non-primate mammals in many domains. CONCLUSION: Comparisons performed in this study demonstrate that birds representing distantly related clades markedly differ in neuronal densities, neuron numbers, and the allocation of brain neurons to major brain divisions. In analogy with the concept of volumetric composition of the brain, known as the cerebrotype, we conclude that distantly related birds have distinct neuronal cerebrotypes.

Department of Anatomy 3rd Faculty of Medicine Charles University Prague Czechia

Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czechia

Department of Zoology Faculty of Science Charles University Prague Czechia

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Emery NJ. Cognitive ornithology: the evolution of avian intelligence. Philos T R Soc B. 2006;361(1465):23–43. PubMed PMC

Güntürkün O, Bugnyar T. Cognition without cortex. Trends Cogn Sci. 2016;20(4):291–303. PubMed

Kabadayi C, Taylor LA, Von Bayern AMP, Osvath M. Ravens, New Caledonian crows and jackdaws parallel great apes in motor self-regulation despite smaller brains. R Soc Open Sci. 2016;3(4):160104. PubMed PMC

Lambert ML, Jacobs I, Osvath M, von Bayern AP. Birds of a feather? Parrot and corvid cognition compared. Behav. 2019;156(5–8):505–94.

Rössler T, Auersperg AM. Recent developments in parrot cognition: a quadrennial update. Anim Cogn. 2023;26(1):199–228. PubMed PMC

Bugnyar T, Reber SA, Buckner C. Ravens attribute visual access to unseen competitors. Nat Commun. 2016;7:10506. PubMed PMC

Kabadayi C, Osvath M. Ravens parallel great apes in flexible planning for tool-use and bartering. Science. 2017;357(6347):202–4. PubMed

Pika S, Sima MJ, Blum CR, Herrmann E, Mundry R. Ravens parallel great apes in physical and social cognitive skills. Sci Rep. 2020;10(1):20617. PubMed PMC

Ksepka DT, Balanoff AM, Smith NA, Bever GS, Bhullar B-AS, Bourdon E, et al. . Tempo and pattern of avian brain size evolution. Curr Biol. 2020;30(11):2026–36.e3. PubMed

Iwaniuk AN, Hurd PL. The evolution of cerebrotypes in birds. Brain Behav Evol. 2005;65(4):215–30. PubMed

Olkowicz S, Kocourek M, Lučan RK, Porteš M, Fitch WT, Herculano-Houzel S, et al. . Birds have primate-like numbers of neurons in the forebrain. Proc Natl Acad Sci U S A. 2016;113(26):7255–60. PubMed PMC

Ströckens F, Neves K, Kirchem S, Schwab C, Herculano-Houzel S, Güntürkün O. High associative neuron numbers could drive cognitive performance in corvid species. J Comp Neurol. 2022;530(10):1588–605. PubMed

Sol D, Olkowicz S, Sayol F, Kocourek M, Zhang Y, Marhounová L, et al. . Neuron numbers link innovativeness with both absolute and relative brain size in birds. Nat Ecol Evol. 2022;6:1381–9. PubMed

Güntürkün O. The avian “prefrontal cortex” and cognition. Curr Opin Neurobiol. 2005;15(6):686–93. PubMed

Nieder A. Inside the corvid brain: probing the physiology of cognition in crows. Curr Opin Behav Sci. 2017;16:8–14.

Nieder A. Convergent circuit computation for categorization in the brains of primates and songbirds. Cold Spring Harb Perspect Biol. 2023;15(12):a041526. PubMed PMC

Güntürkün O, Pusch R, Rose J. Why birds are smart. Trends Cogn Sci. 2024;28(3):197–209. PubMed PMC

von Eugen K, Tabrik S, Güntürkün O, Ströckens F. A comparative analysis of the dopaminergic innervation of the executive caudal nidopallium in pigeon, chicken, zebra finch, and carrion crow. J Comp Neurol. 2020;528(17):2929–55. PubMed

Kverková K, Marhounová L, Polonyiová A, Kocourek M, Zhang Y, Olkowicz S, et al. . The evolution of brain neuron numbers in amniotes. Proc Natl Acad Sci U S A. 2022;119(11):e2121624119. PubMed PMC

Gill F, Donsker DB, Rasmussen PC, editors. IOC World Bird List 12.2 2022.

Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. . Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346(6215):1320–31. PubMed PMC

Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, et al. . A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526(7574):569–73. PubMed

Stiller J, Feng S, Chowdhury A-A, Rivas-González I, Duchêne DA, Fang Q, et al. . Complexity of avian evolution revealed by family-level genomes. Nature. 2024;629(8013):851–60. PubMed PMC

Portmann A. Études sur la cérébralisation chez les oiseaux. Alauda. 1947;15:161–71.

Boire D, Baron G. Allometric comparison of brain and main brain subdivisions in birds. J Hirnforsch. 1994;35(1):49–66. PubMed

Lefebvre L, Whittle P, Lascaris E, Finkelstein A. Feeding innovations and forebrain size in birds. Anim Behav. 1997;53(3):549–60.

Timmermans S, Lefebvre L, Boire D, Basu P. Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol. 2000;56(4):196–203. PubMed

Vallortigara G. The cognitive chicken: visual and spatial cognition in a nonmammalian brain. In: Wasserman EA, Zentall TR, editors. Comparative cognition: experimental explorations of animal intelligence. 2nd ed. Oxford University Press; 2006. p. 53–70.

Marino L. Thinking chickens: a review of cognition, emotion, and behavior in the domestic chicken. Anim Cogn. 2017;20(2):127–47. PubMed PMC

Regolin L, Vallortigara G. Perception of partly occluded objects by young chicks. Percept Psychophys. 1995;57(7):971–6. PubMed

Abeyesinghe SM, Nicol CJ, Hartnell SJ, Wathes CM. Can domestic fowl, Gallus gallus domesticus, show self-control? Anim Behav. 2005;70:1–11.

Meier C, Pant SR, Van Horik JO, Laker PR, Langley EJG, Whiteside MA, et al. . A novel continuous inhibitory-control task: variation in individual performance by young pheasants (Phasianus colchicus). Anim Cogn. 2017;20(6):1035–47. PubMed PMC

Taylor PE, Haskell M, Appleby MC, Waran NK. Perception of time duration by domestic hens. Appl Anim Behav Sci. 2002;76(1):41–51.

Rugani R, Regolin L, Vallortigara G. Discrimination of small numerosities in young chicks. J Exp Psychol Anim Behav Process. 2008;34(3):388–99. PubMed

Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G. Arithmetic in newborn chicks. Proc Biol Sci. 2009;276(1666):2451–60. PubMed PMC

Rugani R, McCrink K, De Hevia M-D, Vallortigara G, Regolin L. Ratio abstraction over discrete magnitudes by newly hatched domestic chicks (Gallus gallus). Sci Rep. 2016;6:30114. PubMed PMC

Kobylkov D, Mayer U, Zanon M, Vallortigara G. Number neurons in the nidopallium of young domestic chicks. Proc Natl Acad Sci USA. 2022;119(32):e2201039119. PubMed PMC

Smith CL, Taylor A, Evans CS. Tactical multimodal signalling in birds: facultative variation in signal modality reveals sensitivity to social costs. Anim Behav. 2011;82(3):521–7.

Gyger M, Marler P. Food calling in the domestic fowl, Gallus gallus: the role of external referents and deception. Anim Behav. 1988;36(2):358–65.

Massen JJM, Hartlieb M, Martin JS, Leitgeb EB, Hockl J, Kocourek M, et al. . Brain size and neuron numbers drive differences in yawn duration across mammals and birds. Commun Biol. 2021;4(1):503. PubMed PMC

Puelles L, Martinez-De-La-Torre M, Paxinos G, Watson C, Martínez S. The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies. 1st ed. Amsterdam; Boston: Academic Press; 2007.

Herculano-Houzel S, Lent R. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci. 2005;25(10):2518–21. PubMed PMC

Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 1992;116(1):201–11. PubMed

Mezey S, Krivokuca D, Bálint E, Adorján A, Zachar G, Csillag A. Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J Comp Neurol. 2012;520(1):100–16. PubMed

Pinheiro J, Bates D, R Core Team. Nlme: linear and nonlinear mixed effects models. 1999:3.1-164.

Upham NS, Esselstyn JA, Jetz W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 2019;17(12):e3000494. PubMed PMC

Herculano-Houzel S, Collins CE, Wong P, Kaas JH. Cellular scaling rules for primate brains. Proc Natl Acad Sci U S A. 2007;104(9):3562–7. PubMed PMC

Gabi M, Collins CE, Wong P, Torres LB, Kaas JH, Herculano-Houzel S. Cellular scaling rules for the brains of an extended number of primate species. Brain Behav Evol. 2010;76(1):32–44. PubMed PMC

Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite REP, et al. . Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol. 2009;513(5):532–41. PubMed

Herculano-Houzel S, Mota B, Lent R. Cellular scaling rules for rodent brains. Proc Natl Acad Sci U S A. 2006;103(32):12138–43. PubMed PMC

Herculano-Houzel S, Ribeiro P, Campos L, Valotta da Silva A, Torres LB, Catania KC, et al. . Updated neuronal scaling rules for the brains of glires (rodents/lagomorphs). Brain Behav Evol. 2011;78(4):302–14. PubMed PMC

Sarko D, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S. Cellular scaling rules of insectivore brains. Front Neuroanat. 2009;3:8. PubMed PMC

Dos Santos SE, Porfirio J, Da Cunha FB, Manger PR, Tavares W, Pessoa L, et al. . Cellular scaling rules for the brains of marsupials: not as “primitive” as expected. Brain Behav Evol. 2017;89(1):48–63. PubMed

Herculano-Houzel S, Manger PR, Kaas JH. Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size. Front Neuroanat. 2014;8:77–28. PubMed PMC

Herculano-Houzel S, Catania K, Manger PR, Kaas JH. Mammalian brains are made of these: a dataset of the numbers and densities of neuronal and nonneuronal cells in the brain of glires, primates, scandentia, eulipotyphlans, afrotherians and artiodactyls, and their relationship with body mass. Brain Behav Evol. 2015;86(3–4):145–63. PubMed

Clark DA, Mitra PP, Wang SS-H. Scalable architecture in mammalian brains. Nature. 2001;411(6834):189–93. PubMed

Lefebvre L, Nicolakakis N, Boire D. Tools and brains in birds. Behav. 2002;139(7):939–73.

Lefebvre L. A global database of feeding innovations in birds. Wilson J Ornithol. 2020;132(4):803–9.

Ngwenya A, Patzke N, Manger PR, Herculano-Houzel S. Continued growth of the central nervous system without mandatory addition of neurons in the nile crocodile (Crocodylus niloticus). Brain Behav Evol. 2016;87(1):19–38. PubMed

Kverková K, Polonyiová A, Kubička L, Němec P. Individual and age-related variation of cellular brain composition in a squamate reptile. Biol Lett. 2020;16(9):20200280. PubMed PMC

Cunha F, Racicot K, Nahirney J, Heuston C, Wylie DR, Iwaniuk AN. Allometric scaling rules of the cerebellum in galliform birds. Brain Behav Evol. 2020;95(2):78–92. PubMed

Cunha F, Gutiérrez-Ibáñez C, Racicot K, Wylie DR, Iwaniuk AN. A quantitative analysis of cerebellar anatomy in birds. Brain Struct Funct. 2021;226(8):2561–83. PubMed

Herculano-Houzel S, Messeder DJ, Fonseca-Azevedo K, Pantoja NA. When larger brains do not have more neurons: increased numbers of cells are compensated by decreased average cell size across mouse individuals. Front Neuroanat. 2015;9:64. PubMed PMC

Marhounová L, Kotrschal A, Kverková K, Kolm N, Němec P. Artificial selection on brain size leads to matching changes in overall number of neurons. Evolution. 2019;73(9):2003–12. PubMed PMC

Cunha F, Stingo-Hirmas D, Cardoso RF, Wright D, Henriksen R. Neuronal and non-neuronal scaling across brain regions within an intercross of domestic and wild chickens. Front Neuroanat. 2022;16:1048261. PubMed PMC

Morterá P, Herculano-Houzel S. Age-related neuronal loss in the rat brain starts at the end of adolescence. Front Neuroanat. 2012;6:45. PubMed PMC

Ebinger P, Röhrs M. Volumetric analysis of brain structures, especially of the visual system in wild and domestic turkeys (Meleagris gallopavo). J Hirnforsch. 1995;36(2):219–28. PubMed

Gutiérrez-Ibáñez C, Iwaniuk AN, Wylie DR. Parrots have evolved a primate-like telencephalic-midbrain-cerebellar circuit. Sci Rep. 2018;8(1):9960. PubMed PMC

Henriksen R, Johnsson M, Andersson L, Jensen P, Wright D. The domesticated brain: genetics of brain mass and brain structure in an avian species. Sci Rep. 2016;6:34031. PubMed PMC

Racicot KJ, Popic C, Cunha F, Wright D, Henriksen R, Iwaniuk AN. The cerebellar anatomy of red junglefowl and white leghorn chickens: insights into the effects of domestication on the cerebellum. R Soc Open Sci. 2021;8(10):211002. PubMed PMC

Racicot KJ, Ham JR, Augustine JK, Henriksen R, Wright D, Iwaniuk AN. A comparison of telencephalon composition among chickens, junglefowl, and wild galliforms. Brain Behav Evol. 2024;99(1):13–24. PubMed

Peterson AT, Brisbin IL. Genetic endangerment of wild red junglefowl Gallus gallus? Bird Conserv Int. 1998;8(4):387–94.

Frahm HD, Rehkämper G. Allometric comparison of the brain and brain structures in the white crested polish chicken with uncrested domestic chicken breeds. Brain Behav Evol. 1998;52(6):292–307. PubMed

Rehkämper G, Kart E, Frahm HD, Werner CW. Discontinuous variability of brain composition among domestic chicken breeds. Brain Behav Evol. 2003;61(2):59–69. PubMed

Tsuboi M, van der Bijl W, Kopperud BT, Erritzøe J, Voje KL, Kotrschal A, et al. . Breakdown of brain–body allometry and the encephalization of birds and mammals. Nat Ecol Evol. 2018;2(9):1492–500. PubMed

Herculano-Houzel S. Numbers of neurons as biological correlates of cognitive capability. Curr Opin Behav Sci. 2017;16:1–7.

Němec P, Osten P. The evolution of brain structure captured in stereotyped cell count and cell type distributions. Curr Opin Neurobiol. 2020;60:176–83. PubMed PMC