Amplification of potential thermogenetic mechanisms in cetacean brains compared to artiodactyl brains

Paul R Manger,Kjell Fuxe,Karl Æ Karlsson,Patrick R Hof,Osama B Mohammed,Mads F Bertelsen,Abdulaziz N Alagaili,Muhammad A Spocter,Suzana Herculano-Houzel,Nigel C Bennett,Adhil Bhagwandin,Nina Patzke

doi:10.1038/s41598-021-84762-0

Abstract

To elucidate factors underlying the evolution of large brains in cetaceans, we examined 16 brains from 14 cetartiodactyl species, with immunohistochemical techniques, for evidence of non-shivering thermogenesis. We show that, in comparison to the 11 artiodactyl brains studied (from 11 species), the 5 cetacean brains (from 3 species), exhibit an expanded expression of uncoupling protein 1 (UCP1, UCPs being mitochondrial inner membrane proteins that dissipate the proton gradient to generate heat) in cortical neurons, immunolocalization of UCP4 within a substantial proportion of glia throughout the brain, and an increased density of noradrenergic axonal boutons (noradrenaline functioning to control concentrations of and activate UCPs). Thus, cetacean brains studied possess multiple characteristics indicative of intensified thermogenetic functionality that can be related to their current and historical obligatory aquatic niche. These findings necessitate reassessment of our concepts regarding the reasons for large brain evolution and associated functional capacities in cetaceans.

Highlights

To elucidate factors underlying the evolution of large brains in cetaceans, we examined 16 brains from 14 cetartiodactyl species, with immunohistochemical techniques, for evidence of non-shivering thermogenesis
UCP1 immunolocalization was observed in neocortical neurons from the occipital and anterior cingulate cortical regions investigated in all cetartiodactyl species examined (Fig. 1, Table 1)
Our analysis revealed that the proportion of immunolabelled UCP1 cortical neurons were significantly different between groups, with the cetaceans studied having a significantly higher proportion of UCP1-immunoreactive neurons in both the occipital cortex (χ2 = 56.30; P = 6.21 × 1 0−14) and anterior cingulate cortex (χ2 = 51.69; P = 6.49 × 10−13) than the artiodactyls studied

Summary

Introduction

To elucidate factors underlying the evolution of large brains in cetaceans, we examined 16 brains from 14 cetartiodactyl species, with immunohistochemical techniques, for evidence of non-shivering thermogenesis. The multiplicity of atypical features of the cetacean brain compared to other mammals includes a homogeneous cerebral cortex[4], an atypical allometric relationship between the brain and body, lack of a layer IV in the entire cerebral cortex, low numbers of cortical areas, paucity of cortical columnar and mini-columnar organization of cortical neurons, a comparatively low number of neuronal morphotypes, a thin and volumetrically small cerebral cortex, a low cortical neuronal density, a high glia:neuron index, altered proportions of the neuropil, a greatly reduced size of the prefrontal c ortex[6], a small hippocampus that lacks adult hippocampal neurogenesis[8], a small corpus callosum[9], unusual and extensive cortical gyrencephaly[10], and low cortical neuronal c omplexity[11] Combined with their unusual sleep p hysiology[12,13], and the finding that cetaceans do not outperform other mammals in behavioural tasks[5,7,14], these features of the cetacean brain mount a significant challenge to the paradigm that cetaceans possess levels of cognitive complexity that differentiate them from the majority of other mammals. Given the presence of UCPs and noradrenaline in the mammalian brain we examined the brains of three species of cetacean and eleven species of the closely related artiodactyls (even-toed ungulates, which combined form the order C etartiodactyla26) to explore the potential cellular basis of the thermogenetic hypothesis of cetacean brain e volution[6]

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Results

Conclusion