Cellular Composition of the Brain of a Northern Minke Whale

Abstract

The largest mammalian brains belong to cetacean species among the cetartiodactyls. Stereological analyses have estimated cetacean numbers of cerebral cortical neurons to be more than the average 16 billion of humans, yet isotropic fractionator estimates in artiodactyls predict that even the largest cetacean brains should have no more than a few billion cortical neurons. Here, we used the isotropic fractionator to investigate these contrasting estimates of neuronal numbers by determining the numbers of neurons and non-neuronal cells forming the brain of a northern minke whale, previously estimated using stereology as containing 12.8 billion cortical neurons (Eriksen and Pakkenberg 2007), and comparing it to our dataset of several dozen mammalian species analyzed with the same method. We report that, with 3.2 billion neurons, the minke whale cerebral cortex conforms to the quantitative scaling rules that apply to other mammals, especially the closely related artiodactyls. The same brain contained a total of 57.4 billion neurons, of which 54.2 billion were cerebellar neurons, matching the expected numbers of a hypothetical artiodactyl brain of similar cerebellar mass. In addition, we found that the northern minke whale brain, with a mass of 2683.9 g, contained 173.4 billion non-neuronal cells, following the universal scaling rules that apply to the brain in all therian mammals examined to date. Thus, how non-neuronal cells are added to the mammalian brain is conserved across therian mammals and is not affected by the transition to an obligatory aquatic life history. Strikingly, we find that the minke whale is an outlier amongst mammals in having almost 18 cerebellar neurons for every neuron in the cerebral cortex, compared to the average ratio of 4, which might be related to infrasonic communication. In addition, with only approximately 88 million neurons, the remainder of the brain (brainstem/diencephalon/subcortical telencephalon) of the northern minke whale exhibited the lowest relative neuronal density of these regions reported in mammalian brains, which might be related to the absence of limbs compared to all other mammalian species. Our results indicate that the number of neurons in cetacean brains has been grossly overestimated by stereological accounts, and place whale brains on par with highly cognitively capable macaws, macaques, baboons, and elephants, but below great apes and humans, in terms of numbers of cortical neurons.