Cellular scaling rules of insectivore brains

Diana Sarko

doi:10.3389/neuro.05.008.2009

Abstract

Insectivores represent extremes in mammalian body size and brain size, retaining various “primitive” morphological characteristics, and some species of Insectivora are thought to share similarities with small-bodied ancestral eutherians. This raises the possibility that insectivore brains differ from other taxa, including rodents and primates, in cellular scaling properties. Here we examine the cellular scaling rules for insectivore brains and demonstrate that insectivore scaling rules overlap somewhat with those for rodents and primates such that the insectivore cortex shares scaling rules with rodents (increasing faster in size than in numbers of neurons), but the insectivore cerebellum shares scaling rules with primates (increasing isometrically). Brain structures pooled as “remaining areas” appear to scale similarly across all three mammalian orders with respect to numbers of neurons, and the numbers of non-neurons appear to scale similarly across all brain structures for all three orders. Therefore, common scaling rules exist, to different extents, between insectivore, rodent, and primate brain regions, and it is hypothesized that insectivores represent the common aspects of each order. The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass. This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass. This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

Highlights

Despite the extensive variation in brain size across mammals that suggests differing cellular composition, computational capacity, and cognitive abilities across species, different mammalian orders have traditionally been pooled together in studies of brain allometry as if their brains were built according to the same scaling rules (e.g., Haug, 1987; Zhang and Sejnowski, 2000)
We found that brain mass (MBR) relates to body mass (MBO) by the power function
We found that total brain mass increases linearly with the number of neurons, the number of non-neurons, and the total number of cells, since brain mass can be described well using either power functions with exponents close to 1 or as linear functions of the number of cells, neurons and non-neurons in the brain

Summary

Introduction

Despite the extensive variation in brain size across mammals (by a factor of approximately 100,000 – Stolzenburg et al, 1989; Tower, 1954) that suggests differing cellular composition, computational capacity, and cognitive abilities across species, different mammalian orders have traditionally been pooled together in studies of brain allometry as if their brains were built according to the same scaling rules (e.g., Haug, 1987; Zhang and Sejnowski, 2000). In the order Rodentia, increased mass of the cerebral cortex, cerebellum, and remaining areas is concurrent with greater numbers of neurons along with even greater numbers of non-neurons, yielding a ratio of non-neurons to neurons that increases with brain size (Herculano-Houzel et al, 2006) These findings corroborated previous studies describing neuronal density decreasing and the glia-to-neuron ratio increasing with increasing brain size across mammalian taxa (Cragg, 1967; Friede, 1954; Haug, 1987; Hawkins and Olszewski, 1957; HerculanoHouzel et al, 2006; Reichenbach, 1989; Shariff, 1953; Stolzenburg et al, 1989; Tower, 1954; Tower and Elliott, 1952; Tower and Young, 1973). The different scaling rules that apply to rodent and primate brains result in the latter being composed of larger numbers of neurons than rodent brains of comparable size, since neuronal density decreases with increasing brain size in rodents but not in primates (Herculano-Houzel et al, 2007)

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