Dogs Have the Most Neurons, Though Not the Largest Brain: Trade-Off between Body Mass and Number of Neurons in the Cerebral Cortex of Large Carnivoran Species.

Débora Jardim-Messeder,Fernanda M Pestana,Abdulaziz N Alagaili,Mads F Bertelsen,Maria E De Castro Leal,Kelly Lambert,Suzana Herculano-Houzel,Stephen Noctor,Osama B Mohammad,Paul R Manger

doi:10.3389/fnana.2017.00118

Abstract

Carnivorans are a diverse group of mammals that includes carnivorous, omnivorous and herbivorous, domesticated and wild species, with a large range of brain sizes. Carnivory is one of several factors expected to be cognitively demanding for carnivorans due to a requirement to outsmart larger prey. On the other hand, large carnivoran species have high hunting costs and unreliable feeding patterns, which, given the high metabolic cost of brain neurons, might put them at risk of metabolic constraints regarding how many brain neurons they can afford, especially in the cerebral cortex. For a given cortical size, do carnivoran species have more cortical neurons than the herbivorous species they prey upon? We find they do not; carnivorans (cat, mongoose, dog, hyena, lion) share with non-primates, including artiodactyls (the typical prey of large carnivorans), roughly the same relationship between cortical mass and number of neurons, which suggests that carnivorans are subject to the same evolutionary scaling rules as other non-primate clades. However, there are a few important exceptions. Carnivorans stand out in that the usual relationship between larger body, larger cortical mass and larger number of cortical neurons only applies to small and medium-sized species, and not beyond dogs: we find that the golden retriever dog has more cortical neurons than the striped hyena, African lion and even brown bear, even though the latter species have up to three times larger cortices than dogs. Remarkably, the brown bear cerebral cortex, the largest examined, only has as many neurons as the ten times smaller cat cerebral cortex, although it does have the expected ten times as many non-neuronal cells in the cerebral cortex compared to the cat. We also find that raccoons have dog-like numbers of neurons in their cat-sized brain, which makes them comparable to primates in neuronal density. Comparison of domestic and wild species suggests that the neuronal composition of carnivoran brains is not affected by domestication. Instead, large carnivorans appear to be particularly vulnerable to metabolic constraints that impose a trade-off between body size and number of cortical neurons.

Highlights

Carnivora is a remarkable order for comparative studies of neuroanatomy because of the wide range of brain and body size of its members, from the smallest, mouse-sized least weasel to the 5-ton Southern elephant seal, overlapping with most other mammalian clades
Notice that the exponent that relates brain mass to body mass across carnivoran species is not significantly different from the exponent that applies to artiodactyls, carnivorans, lion and hyena in particular, have slightly smaller brains than artiodactyl species of similar body mass (Figure 3A; the outlier artiodactyl in the figure is the domesticated pig, which has a very large body mass for its brain mass)
Carnivoran brains have numbers of neurons comparable to those found in non-primate mammals of similar body mass, in particular artiodactyls, cladespecific exponents are again observed (Figure 3B)

Summary

Introduction

Carnivora is a remarkable order for comparative studies of neuroanatomy because of the wide range of brain and body size of its members, from the smallest, mouse-sized least weasel to the 5-ton Southern elephant seal, overlapping with most other mammalian clades. It is tempting to predict that cognitive demand has imposed positive pressure on carnivorans for larger numbers of neurons compared to their prey species, mostly artiodactyls, of similar or even larger body and brain size This possible advantage conferred by larger numbers of neurons, in the cerebral cortex, would have to be balanced by the metabolic cost of having more neurons. Considering that the cerebral cortex is the most expensive structure within the brain (Karbowski, 2007), and that the energetic cost of the brain is proportional to its number of neurons (Herculano-Houzel, 2011), it is conceivable that large meat-eating carnivorans are subject to energetic constraints that might limit their numbers of brain neurons, especially in the cerebral cortex Such a limitation would be expected to appear in the form of a trade-off between body mass and number of brain neurons, as seen in large non-human primates (Fonseca-Azevedo and Herculano-Houzel, 2012)

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