The brains of cats

So 2017 begins on a high for publishing with another paper hot off the presses and long overdue:

Cuff AR, Stockey C, Goswami A, 2017. Endocranial morphology of the extinct North American lion (Panthera atrox). Brain, Behavior and Evolution. DOI: 10.1159/000454705.

To quickly catch everyone up, P. atrox is an extinct lion from North America (as the paper title suggests). The species evolved from a "cave" lion (P. spalaea) population from Eurasia that crossed the Bering Sea around 340,000 years ago. These lion populations in turn split from the lineage that gives rise to the modern lions 1.89 million years ago (Barnett et al., 2016).

Phylogeny of the lion species

A quick note, endocasts are the natural cast (the infilling) of the endocranium (the braincase). In mammals the brain almost entirely fills the cavity so brain and endocast are almost identical (which is why brain swelling is such a major health issues). Birds are similar with their brains filling most of their endocast, but most non-avian dinosaurs and crocodiles have large sinuses that take up large volumes of the endocranium. Prior to our study the only data for P. atrox was from casts of skulls, (where they infilled brain cases with material to produce a cast) carried out in 1932 (Merriam and Stock, 1932). The new study adds some more details to those casts, as well as some additional information on the inner ear (red in the figure below).

From Cuff et al., 2017. Fig. 1. Endocranial reconstruction of P. atrox in left lateral ( a ), right lateral ( b ), dorsal ( c ), and ventral ( d ) views. Anterior is toward the left in a, c, and d and toward the right in b . The endocast is rendered in blue, the inner ear in red, and the cranial nerves in yellow. CN II, optic nerve; CN V 1–3, trigeminal nerve (ophthalmic, maxillary, and mandibular branches); CN VII, facial nerve; CN VIII, vestibulocochlear nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XII, hypoglossal nerve; hy, hypophysis/pituitary; ob, olfactory bulb; ocx, olfactory cortex; pf, paraflocculus; v, vermis. Scale bar = 20 mm. The endocranial orientation in a and b is linked to the likely “alert” head posture

We also compared the morphology of the extinct North American lion to modern Asian/Asiatic lions (below).

From Cuff et al., 2017.Figure 2. Endocranial reconstruction of P. leo persica in A, left lateral; B, right lateral; C, dorsal; and D, ventral views. Anterior is toward the left in A, C, D and toward the right in B. The endocast is rendered in blue, the inner ear in red, and the cranial nerves in yellow.; CN II optic nerve; CN V_1-3, trigeminal nerve (ophthalmic, maxillary and mandibular branches); CN VII facial nerve; CN VIII vestibulocochlear nerve; CN IX, glossopharyngeal nerve; CN X, vagus nerve; CN XII, hypoglossal nerve; hy, hypophysis/pituitary; ob, olfactory bulb; ocx, olfactory cortex; pf, paraflocculus; v, vermis. Scale bar = 20 mm. Endocranial orientation in A and B linked to the likely “alert” head posture. 

Overall the endocasts look fairly similar, but something that you might have noticed is how much more elongate the P. atrox brain looks relative to the modern lion (P. leo). There are some previously published 2D models of some extinct taxa (Radinsky, 1975), with the oldest species showing this similar "elongate" morphology. However, the morphology seen in P. leo where the forebrain sits further back on the hindbrain is more "folded" and was also seen in some of the extinct species (particularly the sabre-tooth cats). So we needed a way to quantify the elongate/folded brain morphology (linked to cephalic flexure), which ended up being a simple ratio of length of hindbrain not covered relative to total brain length (P. atrox and P. leo shown below):

Long line is total length, short line is "exposed" hindbrain not covered by the forebrain.

We however lacked information for many of the extant species on whether the elongate or folded brains were more common and if there were any patterns. Therefore we got hold of a bunch of CT scans from colleagues (Z.J. Tseng, C.Grohé, and J.J. Flynn), and Christopher Stockey (a summer student joined us from Imperial). Chris segmented endocasts from a wide range of extant taxa (see below).

From Cuff et al., 2017. Figure 3. Brain anatomy through Felidae. Proailurus, Pseudaelurus, Dinobastis and Smilodon are all modified from Radinsky[1975]. Phylogeny modified from Piras et al.[2013], total length 27Ma. All scale bars = 2cm.

The results are shown in the table below, with the species with the most elongate brain morphologies with the highest proportion "exposed". P. atrox has 18.6% exposed, whilst P. leo is only 5.9% exposed (actually the lowest we measured). Typically, as with all biology, there is a spectrum rather than a hard and fast rule about the elongation of the brain of felids. Just within the pantherines (Panthera spp. - the big cats) there is a large range in the level of folding. Most of the other living species of cats are fairly consistent in their levels elongation.

Species	Cerebrum and cerebellum length	“Exposed” cerebellum length	Proportion “exposed”
Dinobastis sp.*	0.0979	0.0095	0.097
Smilodon fatalis*	0.0923	0.0124	0.134
Pseudaelurus*	0.0677	0.0165	0.243
Neofelis nebulosi	0.0717	0.0168	0.235
Panthera tigris	0.0999	0.0104	0.104
Panthera pardus	0.0918	0.0160	0.175
Panthera atrox	0.0984	0.0183	0.186
Panthera leo	0.0905	0.0053	0.059
Pardofelis marmorata	0.0550	0.0078	0.142
Carcal aurata	0.0671	0.0093	0.139
Leopardus wiedii	0.0517	0.0065	0.125
Lynx rufus	0.0655	0.0106	0.163
Acinonyx jubatus	0.0697	0.0080	0.115
Puma concolor	0.0855	0.0131	0.154
Prionailurus viverrina	0.0623	0.0108	0.174
Felis silvestris	0.0499	0.0100	0.200
Proailurus*	0.0641	0.0141	0.220

What does this mean? Honestly I don't know. It's a weird quirk of felid morphology that deserves further study, so there is a project if anyone wants to collaborate.

Beyond the crazy brain shapes, what about their sizes? We measured the volume of the endocasts and multiplied it by standard brain tissue density (somewhere between 1.027 g/cm3 [Schröder, 1968] and 1.100 g/cm3 [Barber et al., 1970]). This was this compared to the body size to get a relative brain size.

From Cuff et al., 2017. Figure 4. Regression of log maximum brain mass against log body mass (both in kilograms) for Felidae.

Most cats are fairly similar in relative brain size, with P. atrox slightly above that expected for its body mass. In addition, the absolute brain size (both of this endocast and some of the other P. atrox measured in 1932) is higher than any other felid species measured to date. But what does that mean for the intelligence? Actually in cats there doesn't appear to be an obvious correlation between brain size and sociality with similarly "brainy" cats being capable of both solo living and group living so we cannot say if P. atrox lived in prides like its modern relatives.

References
Barber TEDW, Brockway JA, Higgins LS (1970): The density of tissues in and about the. Acta Neurol Scand 46: 85–92.

Barnett R, Shapiro B, Barnes I, Ho SY, Burger J, Yamaguchi N, et al. (2009): Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity. Mol Ecol Apr;18:1668–1677.

Merriam JC, Stock C (1932): The Felidæ of Rancho La Brea. Washington, Carnegie Institute of Washington.

Radinsky L (1975): Evolution of the felid brain. Brain Behav Evol 11:214–254.

Schröder R (1968): Über das spezifische Gewicht des Hirngewebes in der Nachbarschaft von Tumoren. Aus dem Max-Planck-Institut fur Hirnforschung, Abteilung fur Tumor forschung und expirementelle Pathologie, und der Neurochirurgischen Universitiitsklinik, Koln.