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

Abstract

Comparative studies amongst extant species are one of the pillars of evolutionary neurobiology. In the 20th century, most comparative studies remained restricted to analyses of brain structure volume and surface areas, besides estimates of neuronal density largely limited to the cerebral cortex. Over the last 10 years, we have amassed data on the numbers of neurons and other cells that compose the entirety of the brain (subdivided into cerebral cortex, cerebellum, and rest of brain) of 39 mammalian species spread over 6 clades, as well as their densities. Here we provide that entire dataset in a format that is readily useful to researchers of any area of interest in the hope that it will foster the advancement of evolutionary and comparative studies well beyond the scope of neuroscience itself. We also reexamine the relationship between numbers of neurons, neuronal densities and body mass, and find that in the rest of brain, but not in the cerebral cortex or cerebellum, there is a single scaling rule that applies to average neuronal cell size, which increases with the linear dimension of the body, even though there is no single scaling rule that relates the number of neurons in the rest of brain to body mass. Thus, larger bodies do not uniformly come with more neurons - but they do fairly uniformly come with larger neurons in the rest of brain, which contains a number of structures directly connected to sources or targets in the body.

Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected

“…For example, the mass of the cerebral cortex as well as its neuronal density scale as functions of the number of cortical neurons that are shared across Afrotheria, Glires, Eulipotyphla, and Artiodactyla -but not primates. The latter are characterized by an evolutionarily derived scaling relationship that results in more cortical neurons building a given cortical volume compared to nonprimates [Herculano-Houzel et al, 2014a, 2015a. A similar pattern is found across primate and nonprimate "rest of brain" (RoB; the ensemble of brainstem, diencephalon, and striatum), with more neurons fitting in the primate RoB than in nonprimate structures of a similar mass.…”

“…All collection, dissection, tissue processing, and mathematical procedures were performed as in our previous studies to ensure that all data obtained could be compared directly to those already published for eutherian species [collected in Herculano-Houzel et al, 2015a]. Briefly, brains were either perfused or immersion-fixed with 4% paraformaldehyde, dissected according to similar criteria (as detailed below), and individual brain structures were subjected to isotropic fractionation.…”

“…A similar pattern is found across primate and nonprimate "rest of brain" (RoB; the ensemble of brainstem, diencephalon, and striatum), with more neurons fitting in the primate RoB than in nonprimate structures of a similar mass. Likewise, the mass of the cerebellum as well as its density of neurons scale as shared functions of the number of cerebellar neurons in Afrotheria, Glires, and Artiodactyla, but not in Eulipotyphla and Primata, which appear to have diverged (without the elephant [Herculano-Houzel et al, 2014a, 2015a). Interestingly, regardless of the different scaling of cerebral cortical and cerebellar mass across primates, eulipotyphlans, and other eutherians as these structures gain neurons, neurons are added in evolution at an apparently constant rate of 4 neurons in the cerebellum (Cb) to every neuron in the cerebral cortex (Cx) in a manner that applies across all eutherian species analyzed so far (with the exception of the elephant [Herculano-Houzel, 2010;Herculano-Houzel et al, 2014a]).…”

Universal transition from unstructured to structured neural maps

“…However, it has been shown that sheep show some form of a structured map (61) and that ungulates in general possess similar neuronal scaling rules as rodents (62). The emergence of a structured map in larger rodents is, therefore, likely.…”

You Do Not Mess with the Glia

“…In all of our studies, cerebral cortex includes the hippocampus, all cortex lateral to the rhinal sulcus, and the underlying subcortical white matter; in a growing number of studies, gray and white matter have been examined separately, and that is mentioned explicitly in this review, where applicable. Cerebellum includes the cerebellar peduncles, subcortical white matter, and deep nuclei; rest of brain is the ensemble of hindbrain-midbrain-striatum-diencephalon (not including the cerebellum) [74]. The olfactory bulbs are counted separately, when available, which they often are not due to the difficulty of collecting them intact.…”