Cellular scaling rules for the brain of afrotherians

Abstract

Quantitative analysis of the cellular composition of rodent, primate and eulipotyphlan brains has shown that non-neuronal scaling rules are similar across these mammalian orders that diverged about 95 million years ago, and therefore appear to be conserved in evolution, while neuronal scaling rules appear to be free to vary in evolution in a clade-specific manner. Here we analyze the cellular scaling rules that apply to the brain of afrotherians, believed to be the first clade to radiate from the common eutherian ancestor. We find that afrotherians share non-neuronal scaling rules with rodents, primates and eulipotyphlans, as well as the coordinated scaling of numbers of neurons in the cerebral cortex and cerebellum. Afrotherians share with rodents and eulipotyphlans, but not with primates, the scaling of number of neurons in the cortex and in the cerebellum as a function of the number of neurons in the rest of the brain. Afrotheria also share with rodents and eulipotyphlans the neuronal scaling rules that apply to the cerebral cortex. Afrotherians share with rodents, but not with eulipotyphlans nor primates, the neuronal scaling rules that apply to the cerebellum. Importantly, the scaling of the folding index of the cerebral cortex with the number of neurons in the cerebral cortex is not shared by either afrotherians, rodents, or primates. The sharing of some neuronal scaling rules between afrotherians and rodents, and of some additional features with eulipotyphlans and primates, raise the interesting possibility that these shared characteristics applied to the common eutherian ancestor. In turn, the clade-specific characteristics that relate to the distribution of neurons along the surface of the cerebral cortex and to its degree of gyrification suggest that these characteristics compose an evolutionarily plastic suite of features that may have defined and distinguished mammalian groups in evolution.

Birds have primate-like numbers of neurons in the forebrain

“…1C and Table S2). In line with data from all mammals analyzed so far (32)(33)(34)(35)(36)(37)(38)(39), the densities of nonneuronal (glial and endothelial) cells remain similar across bird species in all brain structures, except for the telencephalon, where nonneuronal cell density appears to be distinctively lower (Fig. 2 D and E).…”

You Do Not Mess with the Glia

“…Importantly, this cell quantification technique has been found by three independent groups to yield results that are comparable to those obtained with unbiased stereology, but are much faster to obtain and far less prone to user error and undersampling [66][67][68]. The consistency of the approach and technique across studies allowed us to collect data that could be compared systematically across structures in individual brains; across individuals of the same species; across species within a clade; across mammalian clades ( Figure 4); and even across mammals, birds, and non-avian reptiles [53][54][55][56][57][58][59][60][61][62][63][64][69][70][71]. While published results have so far been limited to numbers of neuronal and non-neuronal cells, one advantage of the isotropic fractionator is that, because all tissue heterogeneities in cell distribution are literally dissolved, only very small samples are required for counting, which allows for storage of the remaining suspension at −20 • C for later studies employing new markers or morphological criteria [65].…”

“…Over the last 12 years, we and our collaborators have generated a wealth of data on the numbers of neuronal and non-neuronal cells that compose brain structures in over 50 species of mammals [53][54][55][56][57][58][59][60][61][62][63][64]. Our systematic approach to determine the cellular composition of brain structures in a manner that was readily comparable across species, using reproducible dissection criteria, employed a quantitative technique that we developed-the isotropic fractionator [65].…”

“…While that initially appeared to be the case for the cerebral cortex alone, at a time when only a handful of species were analyzed [50], systematic examination of species representing all mammalian clades benefitting from the ease of the isotropic fractionator method showed that neuronal densities do not universally decrease with increasing brain size [53][54][55][56][57][58][59][60][61][62][63][64]-which would have been the requirement for universally increasing GNRs with increasing brain size. Despite the ease with which authors once could claim that the human brain had 10 times more glia than neurons [42,99,100], there are at best similar numbers of neuronal and glial cells in the human brain as a whole [55].…”

Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution

“…Here I examine this second prediction that total sleep duration decreases together with neuronal density mm 22 across mammalian species and in their development. To this end, I present an analysis of a set of 24 species belonging to six mammalian clades for which cortical numbers of neurons, neuronal density and surface area were available [18][19][20][21][22][23][24][25][26][27][28][29], as well as data for total number of sleep hours per day [7]. Data are provided in table 1.…”