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Quantitative Relationships in Delphinid Neocortex

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Quantitative Relationships in Delphinid Neocortex

Heidi S Mortensen et al. Front Neuroanat.

Abstract

Possessing large brains and complex behavioral patterns, cetaceans are believed to be highly intelligent. Their brains, which are the largest in the Animal Kingdom and have enormous gyrification compared with terrestrial mammals, have long been of scientific interest. Few studies, however, report total number of brain cells in cetaceans, and even fewer have used unbiased counting methods. In this study, using stereological methods, we estimated the total number of cells in the neocortex of the long-finned pilot whale (Globicephala melas) brain. For the first time, we show that a species of dolphin has more neocortical neurons than any mammal studied to date including humans. These cell numbers are compared across various mammals with different brain sizes, and the function of possessing many neurons is discussed. We found that the long-finned pilot whale neocortex has approximately 37.2 × 10(9) neurons, which is almost twice as many as humans, and 127 × 10(9) glial cells. Thus, the absolute number of neurons in the human neocortex is not correlated with the superior cognitive abilities of humans (at least compared to cetaceans) as has previously been hypothesized. However, as neuron density in long-finned pilot whales is lower than that in humans, their higher cell number appears to be due to their larger brain. Accordingly, our findings make an important contribution to the ongoing debate over quantitative relationships in the mammalian brain.

Keywords: animal cognition; glia/neuron ratio; neocortical cell density; neocortical cell number; stereology.

Figures

Figure 1
Figure 1
The long-finned pilot whale (Globicephala melas) and its brain. (A) Image of a long-finned pilot whale swimming near the Faroese Islands (copyright Farophoto Inc.). (B) Representative image of a long-finned pilot whale brain.
Figure 2
Figure 2
Anatomy of the long-finned pilot whale brain. Laminar organization in the three regions of interest (not the especially difference in cell density) in (A) the entire neocortex, (B) the primary auditory cortex and (C) the primary visual cortex. (D) Different brain cells. Note the large difference in size of neurons (black arrow) and glial cells (white arrow).
Figure 3
Figure 3
Sampling procedure. (A) After coloring and embedding in agar, the brain was coronally cut into 1 cm thick consecutive slabs. (B) Tissue wedges were sampled from every second slab using SURS. Each wedge was cut into bars, leaving approximately 40 bars. From these 40 bars, 10 bars were subsampled from each region (neocortex, auditory cortex, visual cortex), and embedded in historesin.
Figure 4
Figure 4
Neocortical cell number in individual long-finned pilot whales. Neuron numbers range from 29.1–46.3 × 109, and glial cells range from 99.9–183 × 109. Diamonds indicate neurons, circles indicate glial cells. Abbreviations: AF, adult females (pink), AM, adult males (green), JF, juvenile females (dark red), JM, juvenile males (blue).
Figure 5
Figure 5
Comparative analysis of the long-finned pilot whale neocortex. (A) The long-finned pilot whale is estimated to have the highest number of neocortical neurons than any mammal studied to date, with almost twice as many neurons as humans, as well as (B) the highest number of neocortical glial cells. Similar findings were observed for the (C) primary auditory cortex and (D) visual cortex. Diamonds indicate neurons, circles indicate glial cels.
Figure 6
Figure 6
Expected neuron numbers. (A) Long-finned pilot whales have a higher than expected number of neocortical neurons relative to body weight, although not as high as that for humans or harbor porpoises, and (B) a slightly lower than expected number of neocortical neurons relative to brain weight. Gray shade resembles 95% confidence interval. References: Minke whale (Eriksen and Pakkenberg, 2007), harbor porpoise and harp seal (Walloe et al., 2010), domestic pig (Jelsing et al., 2006), rat (Korbo et al., 1990), Rhesus monkey (macaque) (Christensen et al., 2007), human (Pakkenberg and Gundersen, 1997).

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