Brain size and neuron numbers drive differences in yawn duration across mammals and birds

. 2021 May 06 ; 4 (1) : 503. [epub] 20210506

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33958700
Odkazy

PubMed 33958700
PubMed Central PMC8102614
DOI 10.1038/s42003-021-02019-y
PII: 10.1038/s42003-021-02019-y
Knihovny.cz E-zdroje

Recent studies indicate that yawning evolved as a brain cooling mechanism. Given that larger brains have greater thermolytic needs and brain temperature is determined in part by heat production from neuronal activity, it was hypothesized that animals with larger brains and more neurons would yawn longer to produce comparable cooling effects. To test this, we performed the largest study on yawning ever conducted, analyzing 1291 yawns from 101 species (55 mammals; 46 birds). Phylogenetically controlled analyses revealed robust positive correlations between yawn duration and (1) brain mass, (2) total neuron number, and (3) cortical/pallial neuron number in both mammals and birds, which cannot be attributed solely to allometric scaling rules. These relationships were similar across clades, though mammals exhibited considerably longer yawns than birds of comparable brain and body mass. These findings provide further evidence suggesting that yawning is a thermoregulatory adaptation that has been conserved across amniote evolution.

Zobrazit více v PubMed

Barbizet J. Yawning. J. Neurol. Neurosurg. Psychiatry. 1958;21:203–209. doi: 10.1136/jnnp.21.3.203. PubMed DOI PMC

Baenninger R. Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J. Comp. Psychol. 1987;101:349. doi: 10.1037/0735-7036.101.4.349. DOI

de Vries JIP, Visser GHA, Prechtl HFR. The emergence of fetal behaviour. I. Qualitative aspects. Early Hum. Dev. 1982;7:301–322. doi: 10.1016/0378-3782(82)90033-0. PubMed DOI

Provine RR. Yawning as a stereotyped action pattern and releasing stimulus. Ethology. 1986;72:109–122. doi: 10.1111/j.1439-0310.1986.tb00611.x. DOI

Tesfaye Y, Lal S. Hazard of yawning. Can. Med. Assoc. J. 1990;142:15. PubMed PMC

Smith EO. Yawning: an evolutionary perspective. Hum. Evol. 1999;14:191–198. doi: 10.1007/BF02440156. DOI

Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn? Neurosci. Biobehav. Rev. 2010;34:1267–1276. doi: 10.1016/j.neubiorev.2010.03.008. PubMed DOI

Gallup AC. Why do we yawn? Primitive versus derived features. Neurosci. Biobehav. Rev. 2011;35:765–769. doi: 10.1016/j.neubiorev.2010.09.009. PubMed DOI

Provine RR, Tate BC, Geldmacher LL. Yawning: no effect of 3–5% CO2, 100% O2, and exercise. Behav. Neural Biol. 1987;48:382–393. doi: 10.1016/S0163-1047(87)90944-7. PubMed DOI

Gallup AC, Gallup GG., Jr. Yawning as a brain cooling mechanism: nasal breathing and forehead cooling diminish the incidence of contagious yawning. Evol. Psychol. 2007;5:92–101. doi: 10.1177/147470490700500109. DOI

Gallup AC, Gallup GG., Jr. Yawning and thermoregulation. Physiol. Behav. 2008;95:10–16. doi: 10.1016/j.physbeh.2008.05.003. PubMed DOI

Gallup AC, Eldakar OT. The thermoregulatory theory of yawning: what we know from over 5 years of research. Front. Neurosci. 2013;6:188. doi: 10.3389/fnins.2012.00188. PubMed DOI PMC

Shoup-Knox ML, Gallup AC, Gallup G, McNay EC. Yawning and stretching predict brain temperature changes in rats: support for the thermoregulatory hypothesis. Front. Evol. Neurosci. 2010;2:108. doi: 10.3389/fnevo.2010.00108. PubMed DOI PMC

Gallup GG, Gallup AC. Excessive yawning and thermoregulation: two case histories of chronic, debilitating bouts of yawning. Sleep Breath. 2010;14:157–159. doi: 10.1007/s11325-009-0287-x. PubMed DOI

Eguibar JR, Uribe CA, Cortes C, Bautista A, Gallup AC. Yawning reduces facial temperature in the high-yawning subline of Sprague-Dawley rats. BMC Neurosci. 2017;18:3. doi: 10.1186/s12868-016-0330-3. PubMed DOI PMC

Ramirez V, Ryan CP, Eldakar OT, Gallup AC. Manipulating neck temperature alters contagious yawning in humans. Physiol. Behav. 2019;207:86–89. doi: 10.1016/j.physbeh.2019.04.016. PubMed DOI

Gallup AC, Miller RR, Clark AB. Changes in ambient temperature trigger yawning but not stretching in rats. Ethology. 2011;117:145–153. doi: 10.1111/j.1439-0310.2010.01854.x. PubMed DOI PMC

Gallup AC, Eldakar OT. Contagious yawning and seasonal climate variation. Front. Evolut. Neurosci. 2011;3:3. PubMed PMC

Massen JJM, Dusch K, Eldakar OT, Gallup AC. A thermal window for yawning in humans: yawning as a brain cooling mechanism. Physiol. Behav. 2014;130:145–148. doi: 10.1016/j.physbeh.2014.03.032. PubMed DOI

Eldakar OT, et al. Temperature-dependent variation in self-reported contagious yawning. Adapt. Hum. Behav. Physiol. 2015;1:460–466. doi: 10.1007/s40750-015-0024-6. DOI

Falk D. Brain evolution in Homo: The “radiator” theory. Behav. Brain Sci. 1990;13:333–381. doi: 10.1017/S0140525X00078973. DOI

Kiyatkin EA, Brown PL, Wise RA. Brain temperature fluctuation: a reflection of functional neural activation. Eur. J. Neurosci. 2002;16:164–168. doi: 10.1046/j.1460-9568.2002.02066.x. PubMed DOI

Baker MA. Brain cooling in endotherms in heat and exercise. Annu. Rev. Physiol. 1982;44:85–85. doi: 10.1146/annurev.ph.44.030182.000505. PubMed DOI

Wang H, et al. Brain temperature and its fundamental properties: a review for clinical neuroscientists. Front. Neurosci. 2014;8:307. PubMed PMC

Richie JM. Energetic aspects of nerve conduction: the relationships between heat production, electrical activity and metabolism. Prog. Biophys. Mol. Biol. 1973;26:147–187. doi: 10.1016/0079-6107(73)90019-9. PubMed DOI

Gallup AC, Church AM, Pelegrino AJ. Yawn duration predicts brain weight and cortical neuron number in mammals. Biol. Lett. 2016;12:20160545. doi: 10.1098/rsbl.2016.0545. PubMed DOI PMC

Gallup AC, Crowe B, Yanchus M. Yawn duration predicts brain volumes in wild cats (Felidae) Int. J. Comp. Psychol. 2017;30:1–5. doi: 10.46867/ijcp.2017.30.00.01. DOI

Gallup, A. C., Moscatello, L. & Massen, J. J. M. Brain weight predicts yawn duration across domesticated dog breeds. Curr. Zool. 66, 401–405 (2020). PubMed PMC

Kilgore DL, Bernstein MH, Hudson DM. Brain temperatures in birds. J. Comp. Physiol. 1976;110:209–215. doi: 10.1007/BF00689309. DOI

McKechnie AE, Wolf BO. The physiology of heat tolerance in small endotherms. Physiology. 2019;34:302–313. doi: 10.1152/physiol.00011.2019. PubMed DOI

Bernstein MH, Sandoval I, Curtis MB, Hudson DM. Brain temperature in pigeons: effects of anterior respiratory bypass. J. Comp. Physiol. 1979;129:115–118. doi: 10.1007/BF00798174. DOI

Porter WR, Witmer LM. Avian cephalic vascular anatomy, sites of thermal exchange, and the rete ophthalmicum. Anat. Rec. 2016;299:1461–1486. doi: 10.1002/ar.23375. PubMed DOI

Gallup AC, Miller ML, Clark AB. Yawning and thermoregulation in budgerigars, Melopsittacus undulatus. Anim. Behav. 2009;77:109–113. doi: 10.1016/j.anbehav.2008.09.014. DOI

Gallup AC, Miller ML, Clark AB. The direction and range of ambient temperature change influences yawning in budgerigars (Melopsittacus undulatus) J. Comp. Psychol. 2010;124:133. doi: 10.1037/a0018006. PubMed DOI

Gallup AC, et al. Thermal imaging reveals sizable shifts in facial temperature surrounding yawning in budgerigars (Melopsittacus undulatus) Temperature. 2017;4:429–435. doi: 10.1080/23328940.2017.1373896. PubMed DOI PMC

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;25:2518–2521. doi: 10.1523/JNEUROSCI.4526-04.2005. PubMed DOI PMC

Revell LJ. Size‐correction and principal components for interspecific comparative studies. Evolution. 2009;63:3258–3268. doi: 10.1111/j.1558-5646.2009.00804.x. PubMed DOI

Prinzinger R, Preßmar A, Schleucher E. Body temperature in birds. Comp. Biochem. Phys. A. 1991;99:499–506. doi: 10.1016/0300-9629(91)90122-S. DOI

Jessen, C. Temperature Regulation in Humans and Other Mammals (Springer, 2001).

O’Brien HD. From anomalous arteries to selective brain cooling: parallel evolution of the artiodactyl carotid rete. Anat. Rec. 2020;303:308–317. doi: 10.1002/ar.23987. PubMed DOI

Tattersall GJ, Andrade DV, Abe AS. Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science. 2009;325:468–470. doi: 10.1126/science.1175553. PubMed DOI

Olkowicz S, et al. Birds have primate-like numbers of neurons in the forebrain. Proc. Natl Acad. Sci. USA. 2016;113:7255–7260. doi: 10.1073/pnas.1517131113. PubMed DOI PMC

Iwaniuk AN, Dean KM, Nelson JE. Interspecific allometry of the brain and brain regions in parrots (Psittaciformes): Comparisons with other birds and primates. Brain Behav. Evol. 2005;65:40–59. doi: 10.1159/000081110. PubMed DOI

von Eugen, K., Ströckens, F., Backes, H., Endepols, H., & Güntürkün, O. Glucose Metabolism of the Avian Brain: an FDG-PET Study in Pigeons (Columba livia) with Estimated Arterial Input Function of Anesthetized and Awake State. Poster # 068.12/QQ22 Neuroscience Meeting Planner (Online) (Society for Neuroscience, 2018).

Herculano-Houzel S. Scaling of brain metabolism with a fixed energy budget per neuron: implications for neuronal activity, plasticity and evolution. PLoS ONE. 2011;6:e17514. doi: 10.1371/journal.pone.0017514. PubMed DOI PMC

Kverková K, et al. Sociality does not drive the evolution of large brains in eusocial African mole-rats. Sci. Rep. 2018;8:9203. doi: 10.1038/s41598-018-26062-8. PubMed DOI PMC

Buffenstein R, Yahav S. Is the naked mole-rat Hererocephalus glaber an endothermic yet poikilothermic mammal? J. Therm. Biol. 1991;16:227–232. doi: 10.1016/0306-4565(91)90030-6. DOI

Tucker R. The digging behavior and skin differentiations in Heterocephalus glaber. J. Morphol. 1981;168:51–71. doi: 10.1002/jmor.1051680107. PubMed DOI

McNab BK. The metabolism of fossorial rodents: a study of convergence. Ecology. 1966;47:712–733. doi: 10.2307/1934259. DOI

Stephan H. Methodische Studien über den quantitativen Vergleich architektonischer Struktureinheiten des Gehirns. Z. wiss. Zool. 1960;164:143–172.

Herculano-Houzel S, Mota B, Lent R. Cellular scaling rules for rodent brains. Proc. Natl Acad. Sci. USA. 2006;103:12138–12143. doi: 10.1073/pnas.0604911103. PubMed DOI PMC

Herculano-Houzel S, Collins CE, Wong P, Kaas JK. Cellular scaling rules for primate brains. Proc. Natl Acad. Sci. USA. 2007;104:3562–3567. doi: 10.1073/pnas.0611396104. PubMed DOI PMC

Herculano-Houzel S, et al. Updated neuronal scaling rules for the brains of Glires (rodents/lagomorphs) Brain Behav. Evol. 2011;78:302–314. doi: 10.1159/000330825. PubMed DOI 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;86:145–163. doi: 10.1159/000437413. PubMed DOI

Dos Santos SE, et al. Cellular scaling rules for the brains of marsupials: not as “primitive” as expected. Brain Behav. Evol. 2017;89:48–63. doi: 10.1159/000452856. PubMed DOI

Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S. Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons. Front. Neuroanat. 2014;8:128. doi: 10.3389/fnana.2014.00128. PubMed DOI PMC

Collins CE, et al. Cortical cell and neuron density estimates in one chimpanzee hemisphere. Proc. Natl Acad. Sci. USA. 2016;113:740–745. doi: 10.1073/pnas.1524208113. PubMed DOI PMC

Jardim-Messeder D, et al. Dogs have the most neurons, though not the largest brain: trade-off between body mass and number of neurons in the cerebral cortex of large carnivoran species. Front. Neuroanat. 2017;11:118. doi: 10.3389/fnana.2017.00118. PubMed DOI PMC

Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear-protein in vertebrates. Development. 1992;116:201–211. doi: 10.1242/dev.116.1.201. PubMed DOI

Mezey S, et al. Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus) J. Comp. Neurol. 2012;520:100–116. doi: 10.1002/cne.22696. PubMed DOI

Rehkämper G, Kart E, Frahm HD, Werner CW. Discontinuous variability of brain composition among domestic chicken breeds. Brain Behav. Evol. 2003;61:59–69. doi: 10.1159/000069352. PubMed DOI

Horschler DJ, et al. Absolute brain size predicts dog breed differences in executive function. Anim. Cogn. 2019;22:187–198. doi: 10.1007/s10071-018-01234-1. PubMed DOI

Rogell B, Dowling DK, Husby A. Controlling for body size leads to inferential biases in the biological sciences. Evol. Lett. 2019;4:73–82. doi: 10.1002/evl3.151. PubMed DOI PMC

Gutierrez-Ibanez C, Iwaniuk AN, Wylie DR. Relative brain size is not correlated with display complexity in manakins: a reanalysis of Lindsay et al. (2015) Brain Behav. Evol. 2016;87:223–226. doi: 10.1159/000446312. PubMed DOI

Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 2010;1:3–14. doi: 10.1111/j.2041-210X.2009.00001.x. DOI

Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. The global diversity of birds in space and time. Nature. 2012;491:444–448. doi: 10.1038/nature11631. PubMed DOI

Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Boil. Evol. 2017;34:1812–1819. doi: 10.1093/molbev/msx116. PubMed DOI

Currie, T. E. & Meade, A. In Modern phylogenetic comparative methods and their application in evolutionary biology (ed. Garamszegi, L. Z.) 263–286 (Springer, 2014).

Hadfield JD, Nakagawa S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi‐trait models for continuous and categorical characters. J. Evol. Biol. 2010;23:494–508. doi: 10.1111/j.1420-9101.2009.01915.x. PubMed DOI

Gelman, A. et al. Bayesian Data Analysis (CRC Press, 2013).

McElreath, R. Statistical Rethinking: A Bayesian Course with Examples in R and Stan (CRC Press, 2016).

Lo S, Andrews S. To transform or not to transform: using generalized linear mixed models to analyse reaction time data. Front. Psychol. 2015;6:1171. doi: 10.3389/fpsyg.2015.01171. PubMed DOI PMC

Gelman A, Hwang J, Vehtari A. Understanding predictive information criteria for Bayesian models. Stat. Comput. 2014;24:997–1016. doi: 10.1007/s11222-013-9416-2. DOI

Lemoine NP. Moving beyond noninformative priors: why and how to choose weakly informative priors in Bayesian analyses. Oikos. 2019;128:912–928. doi: 10.1111/oik.05985. DOI

Bürkner PC. brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 2017;80:1–28. doi: 10.18637/jss.v080.i01. DOI

Carpenter B, et al. Stan: a probabilistic programming language. J. Stat. Softw. 2017;76:1–32. doi: 10.18637/jss.v076.i01. PubMed DOI PMC

McShane BB, Gal D, Gelman A, Robert C, Tackett JL. Abandon statistical significance. Am. Stat. 2019;73:235–245. doi: 10.1080/00031305.2018.1527253. DOI

Sawilowsky S. New effect size rules of thumb. J. Mod. Appl. Stat. Methods. 2009;8:467–474. doi: 10.22237/jmasm/1257035100. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...