Greater addition of neurons to the olfactory bulb than to the cerebral cortex of eulipotyphlans but not rodents, afrotherians or primates

Abstract

The olfactory bulb is an evolutionarily old structure that antedates the appearance of a six-layered mammalian cerebral cortex. As such, the neuronal scaling rules that apply to scaling the mass of the olfactory bulb as a function of its number of neurons might be shared across mammalian groups, as we have found to be the case for the ensemble of non-cortical, non-cerebellar brain structures. Alternatively, the neuronal scaling rules that apply to the olfactory bulb might be distinct in those mammals that rely heavily on olfaction. The group previously referred to as Insectivora includes small mammals, some of which are now placed in Afrotheria, a base group in mammalian radiation, and others in Eulipotyphla, a group derived later, at the base of Laurasiatheria. Here we show that the neuronal scaling rules that apply to building the olfactory bulb differ across eulipotyphlans and other mammals such that eulipotyphlans have more neurons concentrated in an olfactory bulb of similar size than afrotherians, glires and primates. Most strikingly, while the cerebral cortex gains neurons at a faster pace than the olfactory bulb in glires, and afrotherians follow this trend, it is the olfactory bulb that gains neurons at a faster pace than the cerebral cortex in eulipotyphlans, which contradicts the common view that the cerebral cortex is the fastest expanding structure in brain evolution. Our findings emphasize the importance of not using brain structure size as a proxy for numbers of neurons across mammalian orders, and are consistent with the notion that different selective pressures have acted upon the olfactory system of eulipotyphlans, glires and primates, with eulipotyphlans relying more on olfaction for their behavior than glires and primates. Surprisingly, however, the neuronal scaling rules for primates predict that the human olfactory bulb has as many neurons as the larger eulipotyphlan olfactory bulbs, which questions the classification of humans as microsmatic.

Conceptual and methodological issues in comparative neuroscience and psychology: a reassessment

“…In particular, while primate species with larger brains have evolved a larger neocortex relative to the size of the cerebellum (Barton 2002), the ratio between their number of neuron appears to have remained constant (Herculano-Houzel 2010). Also, there are discrepancies between the rates at which the neocortex and olfactory bulb gained mass in insectivores and glires compared to the rates at which these structures gained neurons (Ribeiro et al 2014). These results corroborate the adaptative approach discussed here, while emphasising the need for finer analyses since structure size can exaggerate the actual selection on the number of neurons.…”

“…The first is that, depending on the structure or area, the number of neurons will not have the same signification (that is, not the same predictive power) on a structures functional capacity. For example, the fact that the olfactory bulbs in humans contain as many neurons as the largest eulipotyphlan (a mammalian order comprising, among others, shrews and moles) olfactory bulbs has been used to question the classification of humans as microsmatic (Ribeiro et al 2014). While this may be true to some extent (see also Willemet, 2013), the hypothesis above suggests that the number of neurons in the human olfactory bulb does not represent the potential for olfactory abilities because a large part of these neurons may be there only to keep the influence of the olfactory bulb in the human brain, rather than for increasing the olfactory bulb olfactory capacity (Willemet 2015).…”

Poor human olfaction is a 19th-century myth

“…In the mouse the adult bulb volume ranges from 3 to 10 cubic mm across strain and study (46, 47). Across mammalian species the relative volume of the olfactory bulb is negatively correlated with overall brain size (48). Despite these pronounced differences in volume there is little support for the notion that physically larger olfactory bulbs predict better olfactory function, regardless of whether bulb size is considered in absolute or relative terms (36).…”

“…A previous review compiled the number of olfactory bulb neurons across mammalian species across fractionation studies and revisited the issue of proportionality between the number of neurons and overall brain size (48). The graph in Fig.…”

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

“…Through the analysis of 42 species of primates (including the human) [Herculano-Houzel et al, 2007;Azevedo et al, 2009;Gabi et al, 2010;Ribeiro et al, 2014], glires [Herculano-Houzel et al, 2006Ribeiro et al, 2014], eulipotyphlans [Sarko et al, 2009], scandentians [Herculano-Houzel et al, 2007], afrotherians [Herculano-Houzel et al, 2014a;Neves et al, 2014] and artiodactyls [Kazu et al, 2014], we have been able to challenge a number of the initial notions regarding mammalian brain evolution. Specifically, we could show that while there is indeed a shared, single relationship between numbers of nonneuronal cells and the mass of brain structures across species, with relatively unchanging nonneuronal densities, neuronal densities do not vary uniformly across all species and brain structures [reviewed in Herculano-Houzel, 2011a, 2014Herculano-Houzel et al, 2014b], that glia/neuron ratios vary with average neuronal cell size, not brain structure mass, across different brain structures and mammalian species , that the relationship between the number of brain neurons and body mass differs across mammalian orders [Herculano-Houzel, 2011b;Herculano-Houzel et al, 2014b], and that relatively larger cerebral cortices do not hold relatively more of all brain neurons [Herculano-Houzel, 2010;Herculano-Houzel et al, 2014b].…”