Birds have primate-like numbers of neurons in the forebrain Seweryn Olkowicza, Martin Kocoureka, Radek K. Lucanˇ a, Michal Porteša, W. Tecumseh Fitchb, Suzana Herculano-Houzelc,d,1, and Pavel Nemec a,2 aDepartment of Zoology, Faculty of Science, Charles University in Prague, CZ-12844 Prague, Czech Republic; bDepartment of Cognitive Biology, University of Vienna, 1090 Vienna, Austria; cInstituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, CEP 21941-902, Rio de Janeiro, Brazil; and dInstituto Nacional de Neurociência Translacional, Ministério da Ciência e Tecnologia/Conselho Nacional de Pesquisas, CEP 04023-900, São Paulo, Brazil Edited by Dale Purves, Duke University, Durham, NC, and approved May 6, 2016 (received for review August 27, 2015) Some birds achieve primate-like levels of cognition, even though capacity? Not necessarily: it has recently been discovered that their brains tend to be much smaller in absolute size. This poses a the relationship between brain mass and number of brain neu- fundamental problem in comparative and computational neuro- rons differs starkly between mammalian clades (31). Avian science, because small brains are expected to have a lower brains seem to consist of small, tightly packed neurons, and it is information-processing capacity. Using the isotropic fractionator thus possible that they can accommodate numbers of neurons to determine numbers of neurons in specific brain regions, here that are comparable to those found in the much larger primate we show that the brains of parrots and songbirds contain on brains. However, to date, no quantitative data have been avail- average twice as many neurons as primate brains of the same able to test this hypothesis. Here, we analyze how numbers of neurons compare across mass, indicating that avian brains have higher neuron packing – densities than mammalian brains. Additionally, corvids and parrots birds and mammals (32 39) of equivalent brain mass, and de- termine the cellular scaling rules for brains of songbirds and have much higher proportions of brain neurons located in the parrots. Using the isotropic fractionator (40), we estimated the pallial telencephalon compared with primates or other mammals total numbers of neuronal and nonneuronal cells in the cerebral and birds. Thus, large-brained parrots and corvids have forebrain hemispheres, cerebellum, diencephalon, tectum, and brainstem neuron counts equal to or greater than primates with much larger in a sample of 11 parrot species, 13 vocal learning songbird species brains. We suggest that the large numbers of neurons concen- (including 6 corvids), and 4 additional model species representing trated in high densities in the telencephalon substantially contrib- other avian clades (Figs. S1 and S2). Because most of the cited ute to the neural basis of avian intelligence. mammalian studies analyzed cellular composition of only three brain subdivisions, namely the pallium (referred to as the cerebral intelligence | evolution | brain size | number of neurons | birds cortex in those papers), the cerebellum, and rest of brain, we divided the avian brain identically to ensure an accurate com- any birds have cognitive abilities that match or surpass parison of neuronal numbers, densities, and relative distribution those of mammals (1). Corvids and parrots appear to be of neurons in birds and mammals. Specifically, the avian pallium M (comprising the hyperpallium, mesopallium, nidopallium, arcopallium, cognitively superior to other birds, rivalling great apes in many — psychological domains (1–3). They manufacture and use tools (4, and hippocampus) was compared with its homolog the mam- malian pallium (comprising the neocortex, hippocampus, olfac- 5), solve problems insightfully (6), make inferences about causal tory cortices such as piriform and entorhinal cortex, and pallial mechanisms (7), recognize themselves in a mirror (8), plan for future needs (9), and use their own experience to anticipate future behavior of conspecifics (10) or even humans (11), to mention just Significance a few striking abilities. In addition, parrots and songbirds (in- cluding corvids) share with humans and a few other animal Birds are remarkably intelligent, although their brains are groups a rare capacity for vocal learning (12), and parrots can small. Corvids and some parrots are capable of cognitive feats learn words and use them to communicate with humans (13). comparable to those of great apes. How do birds achieve im- Superficially, the architecture of the avian brain appears very pressive cognitive prowess with walnut-sized brains? We in- different from that of mammals, but recent work demonstrates vestigated the cellular composition of the brains of 28 avian that, despite a lack of layered neocortex, large areas of the avian species, uncovering a straightforward solution to the puzzle: forebrain are homologous to mammalian cortex (14–16), con- brains of songbirds and parrots contain very large numbers of form to the same organizational principles (15, 17, 18), and play neurons, at neuronal densities considerably exceeding those similar roles in higher cognitive functions (14, 19), including found in mammals. Because these “extra” neurons are pre- executive control (20, 21). However, bird brains are small and dominantly located in the forebrain, large parrots and corvids the computational mechanisms enabling corvids and parrots to have the same or greater forebrain neuron counts as monkeys achieve ape-like intelligence with much smaller brains remain with much larger brains. Avian brains thus have the potential unclear. The notion that higher encephalization (relative brain to provide much higher “cognitive power” per unit mass than size deviation from brain–body allometry) endows species with do mammalian brains. improved cognitive abilities has recently been challenged by data suggesting that intelligence instead depends on the absolute Author contributions: S.O., M.K., S.H.-H., and P.N. designed research; S.O., M.K., R.K.L., M.P., and number of cerebral neurons and their connections (22–25). This P.N. performed research; R.K.L. and M.P. collected experimental animals; S.O., M.K., S.H.-H., and is in line with recent findings that absolute rather than relative P.N. analyzed data; and S.O., M.K., W.T.F., S.H.-H., and P.N. wrote the paper. brain size is the best predictor of cognitive capacity (26–28). The authors declare no conflict of interest. However, although corvids and parrots feature encephalization This article is a PNAS Direct Submission. comparable to that of monkeys and apes, their absolute brain Freely available online through the PNAS open access option. size remains small (29, 30). The largest average brain size in 1Present address: Department of Psychology and Department of Biological Sciences, corvids and parrots does not exceed 15.4 g found in the common Vanderbilt University, Nashville, TN 37240. raven (29) and 24.7 g found in the hyacinth macaw (30), re- 2To whom correspondence should be addressed. Email: [email protected]. spectively. Do corvids and parrots provide a strong case for re- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. NEUROSCIENCE viving encephalization as a valid measure of brain functional 1073/pnas.1517131113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1517131113 PNAS | June 28, 2016 | vol. 113 | no. 26 | 7255–7260 Downloaded by guest on September 29, 2021 Birds Mammals amygdala) (14–16, 41). The avian subpallium (formed by the A Goldcrest Mouse striatum, pallidum, and septum), diencephalon, tectum, and brain- stem were pooled and compared with the same regions of “ ” 0.36 g 164 0.42 g 71 mammalian brains that are referred to as the rest of brain. The Starling Rat cerebellum is directly compared between the two clades. The results of our study reveal that avian brains contain many more pallial neurons than equivalently sized mammalian brains. 1.86 g 483 1.80 g 200 Rook Marmoset Results Total Numbers of Neurons. We found that the bird brains have more neurons than mammalian brains and even primate brains of similar mass (Fig. 1 A and B), and have very high neuronal densities (Fig. 2 B and C). Among the songbirds studied, weighing 8.36 g 1,509 7.78 g 636 between 4.5 and 1,070 g, brain mass ranges from 0.36 to 14.13 g, Sulphur-crested Cockatoo Galago and total numbers of neurons in the brain from 136 million to 2.17 billion (Fig. S3 and Table S1; for complete data see Datasets S1 and S2). In the parrots studied, body mass ranges between 23 and 1,008 g, brain mass from 1.15 to 20.73 g, and numbers of brain neurons from 227 million to 3.14 billion. Interestingly, the re- 10.1 g 2,122 10.2 g 936 lationship between brain mass and the number of brain neurons x106 x106 can be described by similar power functions in these two bird BC 103 103 A Cerebellum Telencephalon 102 102 Diencephalon Brainstem DN DN Tectum 10 Songbirds 10 Parrots TA Brain mass (g) GG CL TA Primates Brain mass (g) GG Parrots Songbirds Artiodactyls CL B C and other birds 1 Rodents 1 Other birds 106 106 CL 108 109 1010 1011 108 109 1010 1011 GG TA DE# neurons # non-neuronal cells DN 1011 105 105 103 Corvid songbirds Non-corvid songbirds Parrots Primates 10 2 10 10 Artiodactyls 4 Neuronal density (N/mg) 4 Rodents 10 Neuronal density (N/mg) 10 Other birds DN 10 TA 109 DN 110 110 # neurons TA Brain mass (g) Brain mass (g) GG D E Brain mass (g) CL CL GG 1 6 6 108 10 10 CL 10 102 103 104 105 106 10 102 103 104 105 106 GG TA Body mass (g) Body mass (g) DN 105 105 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.