Univerzita Karlova, Přírodovědecká fakulta Katedra zoologie
Doktorský studijní program: Zoologie Autoreferát disertační práce
Evoluce komplexity a procesní kapacity mozku u pták ů : Ř ešení problému pomocí isotropické frak č ní
homogenizace
Evolution of brain complexity and processing capacity in birds: Cracking the problem using isotropic fractionator technique
Mgr. Martin Kocourek
Školitel: Mgr. Pavel Němec, Ph.D.
Praha, 2023
Abstrakt
Nejzákladnějším principem komparativních věd vždy bylo a je hledání podobností a rozdílů.
Proto jsou lidé fascinovaní kognitivními schopnostmi krkavcovitých ptáků a papoušků a jejich podobností s těmi lidskými. Dlouho byla výjimečnost těchto druhů vysvětlována relativní velikostí jejich mozků. Vlastní procesní kapacita však není založena na velikosti mozku, ale na jeho vnitřní architektuře a počtu neuronů a synapsí. Dnes, díky metodě izotropní frakcionace, již máme informace o počtu neuronů u stovek druhů savců, ptáků a plazů.
V této své práci analyzuji zda, a případně jak, se buněčná škálovací pravidla odlišují v rámci třídy ptáci (Aves). Pro ptačí mozek jsou typické velké počty neuronů a s tím související vysoké neurální hustoty, které jsou u hrabavých (Galliformes) srovnatelné s těmi savčími a u pěvců (Passeriformes) a papoušků (Psittaciformes) dokonce převyšují hustoty neuronů pozorované u primátů. Odlišná je také distribuce neuronů. U pěvců a papoušků, a výsledky naznačují, že jde o trend společný pro celou skupinu Telluraves, se největší část neuronů nachází v koncovém mozku, potažmo v palliu. Pro hrabavé, a zdá se že i zbývající ptačí skupiny, je typické, že se většina jejich neuronů nachází v mozečku. Naprostou většinu neuronů mají v mozečku také savci, což by naznačovalo, že se může jednat o ancestrální znak všech blanatých.
Tuto domněnku však vyvrátila analýza buněčného složení mozku u plazů. Pro ně jsou typické mnohem nižší počty neuronů, přičemž velká část se jich nachází v mozkovém kmeni a středním mozku. Ke zvětšení počtu neuronů tedy muselo dojít nezávisle jak u ptáků, tak i u savců. U obou skupin pak můžeme nalézt taxony, u nichž došlo k dalšímu zvětšení počtu neuronů (u ptáků Telluraves, u savců primáti).
Vysoký počet neuronů je výsledkem evolučních tlaků a musí tedy mít své opodstatnění.
Přesto, že neexistuje přímé spojení mezi počtem neuronů a inteligencí, je zřejmé, že tyto spolu často korelují. Příkladem u ptáků může být pozitivní vztah mezi četností výskytu inovativního chování a počtem neuronů, především v palliu ale i v mozečku. Velký mozek s vysokým počtem neuronů nepřináší pouze potenciální adaptivní výhody, ale i náklady spojené s jeho vysokou energetickou náročností. Ta vyžaduje dostatečně vysokou úroveň metabolismu, což se sebou přináší nutnost zbavovat se případného odpadního tepla. Jedním z možných termoregulačních mechanismů je, dle tzv. termoregulační teorie („Brain cooling“), i zívání. Předpoklad, že druhy s větším počtem neuronů budou mít jiné parametry zívání se skutečné podařilo potvrdit – jak u ptáků, tak i u savců byl prokázán pozitivní vztah mezi délkou zívání a počtem neuronů jak v palliu, tak v celém mozku.
Můžeme tedy konstatovat, že ptačí mozek, ač ve srovnání s mozkem většiny savců malý, poskytuje, díky velkému počtu neuronů nahloučených ve vysokých hustotách v koncovém mozku, procesní kapacitu srovnatelnou s tímtéž u savců. Představuje tedy funkčně srovnatelný model uspořádání s mozkem savčím, navíc model velmi prostorově efektivní.
Abstract
The most fundamental principle of comparative sciences has always been and still is the search for similarities and differences. Maybe that is why people are fascinated by the cognitive abilities of birds like corvids and parrots and their similarities to those of humans. For a long time, the prevailing explanation for the unique abilities of these species was their high relative brain size.
However, the brain’s processing capacity is not based on its size but on its internal architecture and the number of neurons and synapses. Today, we already have data on the numbers of neurons for hundreds of mammalian, avian, and reptilian species, obtained with the isotropic fractionator.
In this thesis, I analyse cellular scaling rules for brains of birds and compare them between avian clades. Bird brains are characterized by large numbers of neurons and high neuron densities, which are comparable to those of mammals in gallinaceous birds (Galliformes) and in passerine birds (Passeriformes) and parrots (Psittaciformes) even exceed those observed in primates. The distribution of neurons is also different. In songbirds and parrots, the majority of neurons are typically located in the telencephalon, specifically in the pallium. The latest data suggest that this is a common feature of core land birds (Telluraves). On the other hand, in galliform birds and likely the rest of birds, most neurons are located in the cerebellum. The same is true for mammals and therefore this could be the ancestral condition for all amniotes.
However, analysis of the cellular composition of reptile brains showed that this is not the case.
Brains of non-avian reptiles are characterized by low overall numbers of neurons, with a large proportion of them located in the diencephalon and brainstem. Therefore, increases in the number of neurons must have occurred independently in both birds and mammals.
Interestingly, within both lineages, there are groups that experienced another increase in the number of neurons (Telluraves in birds, primates in mammals).
There must be a reason for having such high numbers of brain neurons. Although there is no direct proof of a link between neuron number and cognitive performance, many studies have shown some correlation between the two. A great example in birds is the positive relationship between the frequency of innovative behaviour and the number of neurons, particularly in the pallium and the cerebellum. At the same time, large brains with high numbers of neurons require a sufficiently high level of metabolism, which brings the need to dissipate extra heat. According to the brain cooling hypothesis, yawning serves at that thermoregulatory mechanism. Our results confirmed the initial hypothesis that species with higher neuron numbers yawn longer. Both birds and mammals show a positive correlation between yawn duration and the number of neurons in the whole brain and in the pallium.
We can conclude that bird brains, although generally smaller than most mammalian brains, have comparable processing capacities, mainly due to the large numbers of neurons concentrated in high densities in the telencephalon. Thus, the avian brain shows a completely different, and spatially effective, way of telencephalic organization.
Introduction
Birds are one of the most diversified group of vertebrates, with almost 11 000 extant species in 253 families and 44 orders (Gill et al., 2022). Their phylogeny remains unsolved, yet the position of some clades is broadly accepted (Jarvis et al., 2014; Prum et al., 2015; Kuhl et al., 2021; Braun & Kimballa, 2021). All extant modern birds are divided into 3 clades: Palaeognathes (ratites and tinamous), Galloanseres (galliform and anseriform birds) and Neoaves (all other birds). Within Neoaves, Reddy et al. (2017) identified seven large clades, whose relationship remain unclear. The most crown clade is Telluraves (core land birds), containing taxa such as woodpeckers, owls, falcons, hawks, parrots, and songbirds.
Core land birds have relatively large brains in comparison to other neoaves (Kverková et al. 2022) and especially songbirds and parrots are well known for cognitive abilities matching those of primates and the great apes (Güntürkün & Bugnyar, 2016;
Lambert et al., 2019). At the same time, avian brains are severalfold smaller compared to brains of great apes (
e.g.,Crile, & Quiring, 1940; Stephan, 1988; Mlíkovský, 1990).
Moreover, the organisation of the forebrain in birds and mammals differ significantly.
Avian pallium and mammalian cortex are not homologous (Briscoe & Ragsdale, 2018;
Medina et al., 2022), although they share similar connectivity patterns (Pfenning et al., 2014; Shanahan et al., 2010), sensory circuits (Colquitt et al., 2021; Stacho et al., 2020) and neuronal populations with analogical molecular and physiological traits (Spool et al., 2021).
On the other hand, songbirds and parrots have much higher brain neuronal densities than mammals in general (Olkowicz et al., 2016) and although there is no direct proof of a link between neuron number and cognitive performance, many studies have shown some correlation between the two (
e.g.,Wright, 2017; Herculano-Houzel et al., 2017). Luckily, Isotropic fractionator provides a relatively fast way of estimating numbers of cells and neuron in whole brains or dissected brain parts (Herculano-Houzel & Lent, 2005). Today, data about numbers of neurons are available for 83 mammalian species (Herculano-Houzel et al., 2015; Dos Santos et al., 2017; Jardim-Messeder et al., 2017;
Kverková et al., 2018; Herculano-Houzel et al., 2020), 111 avian species (Olkowicz et al.,
2016; Kverkova et al., 2022; Kocourek et al., in prep.), 110 reptilian species
(Ngwenya et al., 2016; Storks et al., 2020, Kverková et al., 2022) and the ray-finned fish (guppy; Marhounová et al., 2019).
This comprehensive dataset will hopefully bring a better understanding of the connection between brain and cognition
Aims
The aims of this thesis are:
• To assess the numbers of neurons and glial cells in brains of selected avian clades
• To analyse the cellular scaling rules in these clades
• To use these data to test how neuron numbers affect cognitive and physiological
performance
Materials & methods
Information about the cellular composition of the brain of 245 birds belonging to 111 species were estimated for studies included in the thesis. Animals were overdosed with halothane and perfused transcardially with warmed phosphate-buffered saline followed by cold phosphate-buffered 4% paraformaldehyde solution. Brains were removed, postfixed for an additional 7–21 days, and dissected into the cerebral hemispheres, cerebellum, diencephalon, tectum, and brainstem. In one individual per species, one hemisphere was embedded in agarose and sectioned on vibratome in the coronal plane.
Under oblique transmitted light we manually dissected the pallium from subpallium on each section by cutting along the pallial-subpallial boundary, as defined by Puelles et al.
(2007). The dissected structures were incubated in 30% sucrose solution until they sank, then transferred into antifreeze solution (30% glycerol, 30% Ethylene glycol, 40%
phosphate buffer) and stored at -25°C until further processing.
For each dissected brain division, total numbers of cells, neurons, and nonneuronal cells were estimated following the procedure of isotropic fractionation (Herculano-Houzel & Lent, 2005). After manual homogenization, an isotropic suspension of isolated cell nuclei was stained with the florescent DNA marker DAPI and the total number of nuclei in suspension, and therefore the total number of cells in original tissue, was estimated by determining density of nuclei in small fractions drawn from a homogenate using a Neubauer improved counting chamber. Typically, four 10 µl
aliquots were sampled and coefficient of variation (CV) ≤ 0.10 was achieved. When the(CV) among counts exceeds 0.15, additional aliquots (typically 2–5) were assessed. Once the total cell number was known, the proportion of neurons was determined by immunocytochemical detection of neuronal nuclear marker NeuN (Mullen et al., 1992).
Simultaneously, DAPI-labelled and NeuN-immunopositive nuclei in the Neubauer
chamber were counted. A minimum of 500 nuclei was counted to estimate percentage
of double labelled neuronal nuclei. Numbers of nonneuronal cells were derived by
subtraction.
Publications included in the thesis
I. Olkowicz, S., Kocourek, M., Lučan, R. K., Porteš, M., Fitch, W. T., Herculano-Houzel, S., & Němec, P. (2016). Birds have primate-like numbers of neurons in the forebrain.
Proceedings of the National Academy of Sciences, 113(26), 7255–7260.
http://doi.org/10.1073/pnas.1517131113 (275 citations)
II. Massen, J. J., Hartlieb, M., Martin, J. S., Leitgeb, E. B., Hockl, J., Kocourek, M.,
Olkowicz, S., Zhang Y., Osadnik Ch., Verkleij J.W., Bugnyar T., Němec, P. & Gallup, A.
C. (2021). Brain size and neuron numbers drive differences in yawn duration across mammals and birds. Communications Biology, 4(1), 1-10.
https://doi.org/10.1038/s42003-021-02019-y (15 citations)
III. Sol D., Olkowicz S., Sayol F., Kocourek M., Zhang Y., Marhounová L., Osadnik Ch., Corssmit E.,Garcia-Porta J., Martin T.R., Lefebvre L., Němec P. (2021). Neuron numbers link innovativeness with both absolute and relative brain size in birds.
Nature Ecology & Evolution, 6(9), 1381-1389. https://doi.org/10.1038/s41559-022-01815-x (5 citations)
IV. Kverková, K., Marhounová, L., Polonyiová, A., Kocourek, M., Zhang, Y., Olkowicz, S., Straková, B., Pavelková, Z., Vodička, R., Frynta, D., & Němec, P. (2022). The evolution of brain neuron numbers in amniotes. Proceedings of the National Academy of Sciences, 119(11), e2121624119. https://doi.org/10.1073/pnas.2121624119
(12 citations)
V. Kocourek, M., Zhang, Y., Olkowicz, S., Marhounová, L., Straková, B., Pavelková, Z., Stehlík P., Kušta T., Lučan, R., Hájek, T., Kverková K., & Němec, P. Cellular scaling rules for brains of the galliform birds (Aves, Galliformes) (manuscript in preparation, will be submitted before defense of the thesis)
Results and Discussion
Using isotropic fractionator, we examined the number and distribution of neurons and nonneuronal cells in brains of songbirds, parrots and galliform birds (Publication I &
Publication V). All analysed bird brains are characterized by large numbers of neurons
and high neuron densities, which are comparable to those of mammals. Brains of galliform bird accommodate about half the number of neurons of songbird or parrot brains of the same mass. Neuronal densities in songbirds and parrots even exceed those observed in primates. Also, the relative distribution of neurons among the major brain components differs markedly between these avian clades. Similarly to mammals (Herculano-Houzel et al. 2015), the majority of brain neurons is allocated in the cerebellum of galliform birds, while the telencephalon typically contains less than 35%
of brain neurons. The opposite pattern can be observed in songbirds and parrots, where up to 60-80 % brain neurons is allocated in the telencephalon, specifically in the pallium.
The latest data suggest that galliform birds have less neurons not just in the whole telencephalon, but especially in the associative parts, like the nidopallium and mesopallium (Ströckens et al. 2022). Moreover, the allocation of brain neurons to major brain parts sims to be shared across most of the avian species. There are two different patterns, when galliform birds representing early diverging birds, while songbirds and parrots are representing the core land birds (Publication IV).
According to the brain cooling hypothesis, yawning serves as that thermoregulatory mechanism. We show that yawn duration is associated with the size of the brain, the number of neurons in the whole brain and in the pallium (Publication
II). Interestingly, despite of fact that birds possess higher neuronal numbers (asdescribed above), they exhibited considerably shorter yawns. There are several possible, but not mutually exclusive, explanations. Higher body temperature of birds (Prinzinger et al., 1991) could accelerate the heat exchange, the beak can be used as the heat radiator (Tattersall et al., 2017) and significantly lower energy consumption of an avian neurons suggest, that avian brain produce less heat than mammalian brain with the higher number of neurons (von Eugen et al., 2022).
Number of neurons in pallium and to less extent in cerebellum, could be also
considered a great predictor of the innovativeness of the species (Publication III).
At the same time, an increase in the number of neurons leads to increase of the brain size in both absolute and relative terms and is linked with developmental pattern as was suggested earlier (Striedter & Charvet, 2008; Charvet & Striedter, 2009).
Conclusion
Comparative publications in the thesis provides evidence that the comprehensive dataset of the cellular brain composition bring a new insight into the relationship between the brain size, number of neurons and cognition. At the same time, we described cellular scaling rules for both basal and crown avian clades, show differences in their scaling rules and how they differ from those of mammals.
However, just three avian clades were examined in detail and although some information was shown for another avian species, more detailed analysis is needed.
Especially analysis of clades possesses uncommon ecological or developmental traits, influencing the size of the brain and their cerebrotype. Therefore, I am sure, that future will bring a lot of interesting studies about cellular composition of the avian brain.
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(2022). High associative neuron numbers could drive cognitive performance in corvid species. Journal of Comparative Neurology, 530(10), 1588–1605.
https://doi.org/10.1002/cne.25298
Tattersall, G. J., Arnaout, B., & Symonds, M. R. E. (2017). The evolution of the avian bill as a thermoregulatory organ: Thermoregulatory role of avian bills. Biological Reviews, 92(3), 1630–1656. https://doi.org/10.1111/brv.12299
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Mgr. Martin Kocourek
ORCID iD: 0000-0001-5350-4198
Education:
2013–present: PhD degree in Zoology
Charles University, Faculty of Science, Department of Zoology
Thesis: Evolution of brain complexity and processing capacity in birds:
Cracking the problem using isotropic fractionator technique 2010–2013: Master´s degree in Zoology (Mgr.)
Charles University, Faculty of Science, Department of Zoology Thesis: Cellular scaling roles for passerine brains
2006–2010: Bachelor´s degree in Zoology (Bc.)
Charles University, Faculty of Science, Department of Zoology
Thesis: Development of muscle system and its innervation in the anuran hind-limb.
Employment:
2022–present: Lecturer: Department of Anatomy, Third Faculty of Medicine,Charles University
2010–2013: Researcher: Pavel Němec´s Lab, Department of Zoology, Faculty of Science, Charles University
2006–2010: Researcher: Petr Telenský´s Lab, Department of Physiology, Faculty of Science, Charles University.
Teaching at the Charles University:
2021–present: Structure and function of the human body, Department of Anatomy, 3MF 2015–present: Morphology of animals: Department of Zoology, FS
2017–2020: Ethological methods, Department of Physiology, Faculty of Science
2017–2019: Experimental technics in neurosciences, Department of Physiology, Faculty of Science
List of publications:
4 publications in Scopus database, 307 citations, accessed 20.01.2020 Publications included in the thesis
I. Olkowicz, S., Kocourek, M., Lučan, R. K., Porteš, M., Fitch, W. T., Herculano-Houzel, S., &
Němec, P. (2016). Birds have primate-like numbers of neurons in the forebrain.
Proceedings of the National Academy of Sciences, 113(26), 7255–7260.
http://doi.org/10.1073/pnas.1517131113 (275 citations)
II. Massen, J. J., Hartlieb, M., Martin, J. S., Leitgeb, E. B., Hockl, J., Kocourek, M., Olkowicz, S., Zhang Y., Osadnik Ch., Verkleij J.W., Bugnyar T., Němec, P. & Gallup, A. C. (2021). Brain size and neuron numbers drive differences in yawn duration across mammals and birds. Communications Biology, 4(1), 1-10.
https://doi.org/10.1038/s42003-021-02019-y (15 citations)
III. Sol D., Olkowicz S., Sayol F., Kocourek M., Zhang Y., Marhounová L., Osadnik Ch., Corssmit E.,Garcia-Porta J., Martin T.R., Lefebvre L., Němec P. (2021). Neuron numbers link innovativeness with both absolute and relative brain size in birds. Nature Ecology
& Evolution, 6(9), 1381-1389. https://doi.org/10.1038/s41559-022-01815-x
(5 citations)
IV. Kverková, K., Marhounová, L., Polonyiová, A., Kocourek, M., Zhang, Y., Olkowicz, S., Straková, B., Pavelková, Z., Vodička, R., Frynta, D., & Němec, P. (2022). The evolution of brain neuron numbers in amniotes. Proceedings of the National Academy of Sciences, 119(11), e2121624119. https://doi.org/10.1073/pnas.2121624119 (12 citations) V. Kocourek, M., Zhang, Y., Olkowicz, S., Marhounová, L., Straková, B., Pavelková, Z.,
Stehlík P., Kušta T., Lučan, R., Hájek, T., Kverková K., & Němec, P. Cellular scaling rules for brains of the galliform birds (Aves, Galliformes). (Manuscript in preparation, will be submitted before defense of the thesis)
Publications not included in the thesis
VI. Jindrová, M., Kocourek, M., & Telenský, P. (2020). Skin conductance rise time and amplitude discern between different degrees of emotional arousal induced by affective pictures presented on a computer screen. bioRxiv.
https://doi.org/10.1101/2020.05.12.090829
VII. Pátková, Ž., Třebický, V., Kocourek, M., Schwambergová D., Kleisner, K., Havlíček, J., Třebická Fialová, J. Sex and context-dependent differences in visual attention to faces.
(in prep.)
Selected lectures and posters:
2019 Developmental mechanisms underlying enlargement of the telencephalon differ in their potential to generate large neuronal populations: a case of galliform and anseriform birds. Kocourek M., Zhang Y., Osadnik Ch., Kersten Y., Olkowicz, S. & Němec P.
(International Congress of Vertebrate Morphology, Prague) poster presentation Cellular scaling rules for brains of Paleognath birds: Implications for the evolution of avian brains. Kocourek M., Olkowicz S., Zhang Y. & Němec P. (9th European Conference on Comparative Neurobiology, Murcia) poster presentation
2018 Cellular scaling rules for brains of galliform (Galliformes) and anseriform birds (Anseriformes). Kocourek M., Zhang Y., Osadnik Ch., Kersten Y., Olkowicz, S. & Němec P. (9th European Conference on Behavioural Biology, Liverpool) poster presentation Kvantitativní buněčné složení ptačích mozků je taxonově specifické. Kocourek M., Olkowicz S., Zhang Y., Marhounová L., Osadnik Ch. & Němec P. (Zoologické dny, Praha) talk
2017 Srovnání škálovacích pravidel mozku u ptáků a savců. Kocourek M., Olkowicz S., Zhang Y., Marhounová L., Osadnik Ch. & Němec P. (44. Konference České a slovenské
etologické společnosti, Jihlava) talk
2016 Kvantitativní analýza buněčného složení mozku hrabavých. Kocourek M., Zhang Y., Olkowicz S. & Němec P. (Zoologické dny, České Budějovice) talk
2015 Pravidla buněčného škálování mozku v ptačí říši. Kocourek M., Zhang Y., Osadnik Ch., Olkowicz S. & Němec P. (Kostelecké inspirování, Kostelec nad Černými lesy) talk
