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

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Carnivorans are a divers group of mammals that includes carnivorous, omnivorous and herbivorous, domesticated and wild species, with a big scope of mind sizes. Carnivory is one of respective factors expected to be cognitively demanding for carnivorans due to a necessity to outsmart larger raven. On the other hand, large carnivoran species have high hunt 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 genius neurons they can afford, specially in the cerebral lens 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 ( kat, mongoose, frank, hyena, lion ) share with non-primates, including even-toed ungulate ( the typical raven of big carnivorans ), roughly the same relationship between cortical mass and number of neurons, which suggests that carnivorans are subject to the lapp evolutionary scale rules as other non-primate clades. however, there are a few authoritative exceptions. Carnivorans stand out in that the usual relationship between larger body, larger cortical batch 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 deprive hyena, african lion and even brown behave, flush though the latter species have up to three times larger cortices than dogs. signally, the brown bear cerebral cortex, the largest examined, merely has arsenic many neurons as the ten-spot times smaller vomit cerebral cerebral cortex, although it does have the expected ten times vitamin a many non-neuronal cells in the cerebral cortex compared to the guy. We besides find that raccoons have dog-like numbers of neurons in their cat-sized brain, which makes them comparable to primates in neural density. Comparison of domestic and wild species suggests that the neural composition of carnivoran brains is not affected by domestication. rather, large carnivorans appear to be particularly vulnerable to metabolic constraints that impose a tradeoff between torso size and number of cortical neurons .

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. Carnivoran brains are highly convoluted, although less so than cetartiodactyl and archpriest brains of similar mass ( Pillay and Manger, 2007 ; Manger et al., 2010 ). Carnivorans are besides highly diverse : they can be social or solitary confinement animals ; carnivorous, omnivorous, or even frugivorous ; domestic ( such as cats and dogs ) or wild .
Carnivory comes with costs and benefits that are probably to impose a delicate balance on the relationship between brain and body. Although meat eat ( and therefore hunt ) is not universal among carnivorans, search is a have of this clade that might impose a larger cognitive demand on the brain than its counterpart : being preyed upon, since prey species tend to find safety in numbers. It is frankincense tempting to predict that cognitive demand has imposed positive pressure on carnivorans for larger numbers of neurons compared to their prey species, largely even-toed ungulate, of similar or evening larger body and brain size. however, this potential advantage conferred by larger numbers of neurons, peculiarly in the cerebral cortex, would have to be balanced by the metabolic monetary value of having more neurons. daily sleep prerequisite and dietary message are key elements here. While even-toed ungulate afford big bodies through a boastfully time investment in feeding on plant leaves of low thermal content ( Du Toit and Yetman, 2005 ), an investment made possible by brains that can do with american samoa few as 3 heat content of sleep per day ( Zepelin and Rechtschaffen, 1974 ), carnivorans typically are nonoperational, possibly asleep, over 12 h per sidereal day ( Zepelin and Rechtschaffen, 1974 ). furthermore, carnivorous species have highly variable star feeding success ( Gorman et al., 1998 ), and hunting comes at a peculiarly high metabolic monetary value for the largest marauder species ( Carbone et al., 2007 ), factors which are likely to be a indebtedness for a weave such as brain that has a systematically high metabolic prerequisite, and is one of the most expensive tissues of the body ( Aschoff et al., 1971 ). Considering that the cerebral cortex is the most expensive structure within the mind ( Karbowski, 2007 ), and that the energetic cost of the brain is proportional to its total of neurons ( Herculano-Houzel, 2011 ), it is conceivable that large flesh-eating carnivorans are particularly subject to energetic constraints that might limit their numbers of brain neurons, particularly in the cerebral lens cortex. Such a limit would be expected to appear in the imprint of a tradeoff between consistency batch and numeral of brain neurons, as seen in large non-human primates ( Fonseca-Azevedo and Herculano-Houzel, 2012 ) .
Carnivorans are divided into two independent suborders, Caniformia and Feliformia, both of which include species that were domesticated, which has been suggested to alter the relationship between brain and body size ( Kruska, 2007 ). In phylogenetic terms, carnivorans are closely related to artiodactyls ( Bininda-Emonds et al., 2007 ), animals that the large flesh-eating carnivorans prey upon. We have previously found that even-toed ungulate share with marsupials, afrotherians, glires, and eulipotyphlans the scale relationship between act of cortical neurons and decreasing median neural concentration in the cerebral lens cortex ( which reflects larger modal neural cell sizes ; Mota and Herculano-Houzel, 2014 ), such that the mass of the cerebral lens cortex scales faster than the cortex gains neurons across species ( reviewed in Herculano-Houzel, 2016 ). Primates, on the early hand, have larger neural densities in the cerebral lens cortex than non-primates of exchangeable cortical mass ( Herculano-Houzel, 2016 ), and therefore larger numbers of neurons in similarly sized structures, which we have proposed to convey a cognitive advantage to primates ( Herculano-Houzel, 2012 ). The relationship between consistency aggregate and number of brain neurons is highly variable in a clade-specific manner, but it is improbable to contribute to cognitive capabilities across species ( Herculano-Houzel, 2017 ). In contrast, all mammal species examined so far partake the same kinship between the aggregate of major mind structures and the numbers of non-neuronal cells that compose them ( Herculano-Houzel, 2014 ; Dos Santos et al., 2017 ), which indicates that a individual scale rule has governed the addition of non-neuronal cells to brain weave for at least 166 million years ( Murphy et al., 2001, 2004 ; Bininda-Emonds et al., 2007 ).

hera we determine the cellular composing of the mind of eight carnivoran species ( ferret out, banded mongoose, raccoon, domestic kat, domestic frump, striped hyena, lion, and brown bear ) to investigate several possibilities : ( 1 ) that all carnivoran brains and substructures follow the same non-neuronal scale rules that apply to all other therians examined so far, with alike non-neuronal cellular telephone densities ; ( 2 ) that different neural scale rules apply to carnivoran brains compared to other non-primate brains, in particular such that carnivoran brains have more neurons than even-toed ungulate brains of like mass ; ( 3 ) that domesticated species diverge from hazardous species in their neural typography and kinship to body mass ; and ( 4 ) that carnivoran brains exhibit evidence of an energetic tradeoff between body mass and number of brain neurons, particularly in the cerebral cerebral cortex .

Materials and Methods

here we use the isotropic fractionator ( Herculano-Houzel and Lent, 2005 ; Herculano-Houzel, 2012 ) to determine the numbers of neural and non-neuronal cells that compose the main structures ( olfactory light bulb, hippocampus, cerebral cerebral cortex, cerebellum and lie of brain ) of eight carnivoran species. The isotropic fractionator consists of dissolving brain tissue in a detergent solution to collect all cell nucleus in a suspension that can be made isotropic by agitation. Numbers of nuclei are determined by counting DAPI-stained samples under a fluorescent microscope ; numbers of neurons are then calculated after determining the fraction of cell nucleus that express NeuN, a universal joint neural nuclear marker ( Mullen et al., 1992 ). While some specific neural populations fail to express NeuN, such as mitral cells in the olfactory medulla oblongata and Purkinje cells in the hippocampus, those populations are negligible for the purpose of determining total numbers of neurons in the major mind structures and comparing them across species. importantly, the isotropic fractionator has been shown to yield results that are comparable to those obtained with well-employed stereological techniques, and in less time ( Herculano-Houzel et al., 2015b ), which is fundamental for the analysis of large brains .

Animals

We analyzed one brain hemisphere of one or two individuals of the following eight species : domestic black-footed ferret ( Mustela putorius furo, n = 2 ), banded mongoose ( Mungos mungo, n = 1 ), raccoon ( Procyon lotor, n = 2 ), caterpillar ( Felis catus, n = 1 ), andiron ( Canis familiaris, n = 2 ), striped hyena ( Hyaena hyaena, n = 1 ), african lion ( Panthera leo, n = 1 ) and brown hold ( Ursus arctos, n = 1 ). These species are divided into the suborders Caniformia ( ferret, raccoon, chase, brown bear ) and Feliformia ( cat, banded mongoose, striped hyena, leo ; Figure 1 ). Ferret, computerized tomography and pawl individuals were bred in captivity, and are considered to represent domestic species ; the banded mongoose, african leo and embrown behave specimens were obtained from the Copenhagen Zoo after being euthanized with sodium pentobarbital sodium ( i.v ) in line with management decisions of the menagerie ; raccoons were wild caught in Cook County, IL, United States, with license from The Cook County Forest Preserve Field Office in Chicago, IL, United States as separate of their routine pathogen surveillance caparison ; the striped hyena specimen was from an pornographic female that was obtained from the Saudi Wildlife Authority following veterinarian euthanasia for unrelated aesculapian reasons. Cat and dogs were donated by their owners after the natural death of the animals from non-neurological causes, with approval of the Federal University of Rio de Janeiro Committee for Ethics in the Use of Animals ( serve number 01200.001568/2013-87 ). The animals obtained from the Copenhagen Zoo and from Saudi Arabia were treated and used according to the guidelines of the University of Witwatersrand Animal Ethics Committee ( clearance number 2012/53/1 ), which represent with those of the NIH for care and use of animals in scientific experiment. All other animals were killed by overdose with anesthetics according to NIH ( ferrets, raccoons ) and brazilian ( cats and dogs ) veterinary guidelines. once dead, the heads of the larger species were removed from the soundbox and were perfused through the carotid arteries with a rinse of 0.9 % saline ( 0.5 l/kg mass ), followed by fixation with of 4 % paraformaldehyde in 0.1 M phosphate buffer ( PB ) ( 1 lambert /kg mass ) ( Manger et al., 2009 ). Ferrets, mongoose and raccoons were perfusion fixed through the heart ; striped hyena, guy and dog brains were only immersion-fixed once removed from the skull. All other brains were removed from the skull after perfusion and post-fixed ( in 4 % paraformaldehyde in 0.1 M PB ) for 24–72 heat content at 4°C. The brains were then transferred to a solution of 30 % sucrose in 0.1 M PB at 4°C until they had equilibrated and were then transferred to an antifreeze solution containing 30 % glycerol, 30 % ethylene diol, 30 % condense water and 10 % 0.244 M PB. once again the brains were allowed to equilibrate in the solution at 4°C and were then moved to a -20°C deep-freeze for storage prior to use in the current experiments. Cat and pawl brains were fixed by concentration in 4 % paraformaldehyde in 0.1M phosphate buffer for a total of approximately 2 weeks .

FIGURE 1

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FIGURE 1. Phylogenetic relationships across the carnivoran species studied. Four of the species belong to the suborder Caniformia ( frank, raccoon, ferret out and brown wear ), and four to the family Feliformia ( striped hyena, banded mongoose, leo and cat ) .

Brains were removed, cut into left and right halves, one of which was preserved for subsequently histological studies, and the other used for quantification with the isotropic fractionator. When available ( alone for one raccoon and two ferrets ), the olfactory bulb ( OB ) was first base separated from the brain by transection immediately proximal to the main bulb. The cerebellum ( CB ) was dissected by cutting the peduncles at the airfoil of the brainstem. The brainstem was separated from the cerebrum by cutting along a plane front tooth to the colliculi and posterior to the hypothalamus. The cerebrum was then cut into a series of 2 millimeter wreath sections, which were imaged on a flatbed scanner for subsequent morphometric analysis. From these sections, the hippocampus ( HP ) and the corps de ballet of diencephalon + corpus striatum were removed, and the remaining cerebral cortex ( CX ) was then separated into grey and egg white matter components in each section. Although counted individually, in the award learn we concern ourselves entirely with the sum of gray and white cortical matter, to which we besides add the hippocampus ( CxT ), for the sake of comparison with previous studies on other mammalian species ( data provided in Herculano-Houzel et al., 2015a ). As in those studies, the corps de ballet of brainstem and diencephalon + corpus striatum is reported here as the rest of brain ( RoB ), and whole brain ( BR ) refers to the summarize of CxT, CB and RoB ( that is, it excludes the olfactory bulb, for the sake of consistency, since the olfactory light bulb is frequently not available for analysis ; Herculano-Houzel et al., 2015a ). Each social organization was weighed anterior to homogenization. All values in tables and graph equate to masses and cell act estimates ( or averages, where two individuals were available ) multiplied by two, to represent both sides of the brain, as in our former studies ( Herculano-Houzel et al., 2015a ). This operation assumes that any differences between two sides of the brain are negligible compared to the differences across species that span several orders of magnitude in mind structure mass and numbers of cells in the present discipline .

Morphometry

Images of all wreath sections of the cerebral cortex were imported into StereoInvestigator software ( MBF Bioscience, Williston, VT, United States ) for tracing and reconstruction of sum and exposed cortical surface areas, and for Cavalieri analysis to determine grey and white matter volumes, using formulas described previously ( Ribeiro et al., 2013 ; Kazu et al., 2014 ). The median thickness of the gray count was calculated as the ratio between entire gray matter book and surface area, and the folding index of the whole lens cortex was calculated as the ratio between full grey matter surface area and exposed cortical open area, as in a previous study of cortical fold ( Mota and Herculano-Houzel, 2015 ) .

Isotropic Fractionator

After weighing, each structure was sliced by hand and dissolved in a solution of 1 % Triton X-100 in 30 millimeter sodium citrate in a glass Tenbroeck homogenizer ( Pyrex, Corning, NY, United States ) until no visible particles remained. The homogenate and respective washes of the homogenizer were collected in a calibrate cylinder to which DAPI ( 4,6-diamidino-2-phenylindole, Invitrogen, United States ) was added in a dilution of 1:20 to 1:50 from a stock solution of 20 mg/l. The bulk of the suspension was rounded up with PBS to a measure that could be read with preciseness on the calibrated cylinder. After agitating the suspension, with care not to form bubbles, typically four aliquots were taken and placed on Neubauer improved chambers for counting under a fluorescent microscope ( Zeiss, Jena, Germany ). typically, numbers of nuclei were counted in volumes of either 40 or 100 nl on the chambers, whichever sufficed to ensure that at least 60 but not more than 300 nuclei were counted per aliquot. Four aliquots were considered sufficient for a dependable estimate when they yielded a coefficient of variation ( CV ) of less than 0.15. typically, CVs were well below 0.10. Isotropic fractionation frankincense provides estimates of numbers of cells that are at least ampere reliable as those obtained with stereology ( Herculano-Houzel et al., 2015b ). importantly, the modest CVs mean that our estimates of cell numbers have standard deviations of less than 10 % of the appraisal for each specimen, in contrast to the variation of orders of magnitude across species, which is crucial given that we much have only one specimen of each species available for analysis .
A sample distribution of 500 μl of each suspension was then washed in phosphate-buffered saline solution ( PBS ) and reacted overnight with Cy3-conjugated rabbit polyclonal anti-NeuN antibody ( ABN78C3, Millipore, United States ) at room temperature. The adjacent day, samples were washed and resuspended in PBS, and stained again with a 1:20–1:50 dilution of the broth solution of DAPI. One aliquot of each sample was then inspected under the fluorescence microscope for counting the divide of at least 500 DAPI-labeled nucleus that besides exhibited NeuN immunoreactivity. This divide was multiplied by the total number of nucleus ( and consequently cells ) previously obtained in that structure to yield the total total of neurons. This procedure was followed for all species except for the hyena, whose mind had been fixed in paraformaldehyde besides long to allow immunohistochemistry. In this species, the divide of neural nucleus was determined according to morphologic criteria : nucleus were considered to belong to neurons if they were round ( freelancer of size ), exhibited loosen chromatin and a individual nucleolus. The numeral of non-neuronal cells was obtained by subtracting the total of neurons from the sum count of cells. Densities of neural and non-neuronal cells correspond to the issue of the respective cells in the structure divided by the mass of the structure in milligrams ( cells/mg ) .

Mathematical Analyses

All analyses were performed in JMP 9.0 ( SAS, Cary, NC, United States ). Power functions were calculated by fitting a analogue function to log-transformed data using least-squares arrested development. All analyses are performed individually for each mammal clade ; clades are pooled alone when regression analyses show that scaling relationships are described by similar functions. Values obtained for carnivoran species ( n = 8 ) were compared to those predicted for other non-primate mammalian species in our dataset ( n = 37 ) to test whether carnivorans conform to the non-primate mammal scaling rules for different brain structures in relation to numbers of cells and to body mass. The character of phylogenetic bunch is examined directly by performing each analysis individually by clade. We do not use methods to account for phylogenetic relatedness within each clade because our main concenter is on scaling relationships between numbers of cells, cellular telephone density and structure mass arsenic well as their absolute numbers in key species, regardless of any make bold phylogenetic relationships among them. All raw data are provided sol that those concern in testing these relationships within clades may do so .

Results

In our sample of carnivoran species, body multitude varied 437.5-fold between ferret and brown give birth, the smallest and largest species examined, whereas brain batch varied only 58.0-fold, and the total number of neurons in the genius entirely 23.7-fold, between the same two species ( Figure 2 and Table 1 ). The discrepancy between the boastfully variation in body aggregate and numeral of genius neurons is consistent with the vogue that we have revealed of much fast increases in body mass than in numbers of brain neurons ( Herculano-Houzel, 2017 ). furthermore, the larger addition in brain bulk than in number of neurons across species is a inaugural indication that larger brains have more but besides bigger neurons, as found in non-primate species ( Herculano-Houzel et al., 2014b ). Data are summarized in mesa 1 .

FIGURE 2

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FIGURE 2. Examples of brain hemispheres of the carnivoran species studied. Images show the median view of one half-brain ( not inevitably the right half as the images suggest ; some are mirror-images for conformity ). All images are shown to the lapp scale ( scale bar, 1 centimeter ) .

table 1

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TABLE 1. Summary of the cellular constitution of the major brain structures of eight carnivoran species .

Carnivorans have brain masses in the lapp range as other non-primate mammals of alike body mass, including even-toed ungulate, although the power function that relates brain multitude to soundbox mass has a smaller exponent of 0.608 ± 0.051 in carnivorans ( Figure 3A ) compared to 0.712 ± 0.071 in glires, 0.742 ± 0.061 in marsupials, 0.903 ± 0.082 in primates ( all exponents have p -values < 0.0001 ), but is not importantly different from the advocate of 0.548 ± 0.038 ( p = 0.0048 ) in even-toed ungulate ( unfilled symbols in Figure 3A ). Notice that although the exponent that relates brain bulk to body mass across carnivoran species is not importantly different from the exponent that applies to artiodactyls, carnivorans, lion and hyena in particular, have slenderly smaller brains than even-toed ungulate species of similar body mass ( Figure 3A ; the outlier artiodactyl in the calculate is the domesticate farrow, which has a very bombastic body multitude for its brain bulk ). hush, carnivoran brains have numbers of neurons comparable to those found in non-primate mammals of like body batch, in particular even-toed ungulate, although clade-specific exponents are again note ( Figure 3B ). For exemplify, the lion and hyena, at a sum 3.9–4.7 billion neurons, have the same stove of brain neurons as the blesbok and greater kudu, at 3.0–4.9 billion neurons ( Herculano-Houzel et al., 2015a ) .

FIGURE 3

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FIGURE 3. Structure bulk and total of neurons scale with body batch across carnivoran species, except for the total of neurons in the cerebral cerebral cortex. Plotted functions, in bolshevik, apply to carnivoran species and include the 95 % confidence time interval for the fit. Carnivoran species analyzed in this study are shown in colors according to the key in the graph ; non-carnivoran species are depicted in grey ( primates in triangles, even-toed ungulate as unfilled circles ). (A) Brain mass scales as a world power officiate of body mass with advocate 0.608 ± 0.051 across carnivoran species ( r 2 = 0.959, p < 0.0001, n = 8, plotted ), which is not significantly different from the exponent of 0.548 ± 0.038 that applies across even-toed ungulate ( r 2 = 0.990, p = 0.0048, n = 4 ), but is significantly lower than the exponent that applies across primates ( 0.903 ± 0.082, r 2 = 0.931, p < 0.0001, n = 11 ). (B) The numeral of neurons in the genius scales as a exponent officiate of body mass with exponent 0.492 ± 0.054 across carnivoran species ( r 2 = 0.932, p = 0.0001, n = 8, plotted ), which is indistinguishable from the exponent of 0.448 ± 0.115 that applies across even-toed ungulate ( r 2 = 0.884, p = 0.0598, n = 4 ), but is importantly lower than the exponent of 0.777 ± 0.091 ( r 2 = 0.889, p < 0.0001, n = 11 ) that applies across primates. (C) The mass of the cerebral lens cortex of carnivorans scales as a might function of body mass with exponent 0.631 ± 0.062 ( r 2 = 0.944, p < 0.0001, n = 8, plotted ), which is not importantly different from the exponent that applies across artiodactyl species ( 0.589 ± 0.028, r 2 = 0.995, p = 0.0023, n = 4 ), although smaller than the advocate that applies across primate species ( 0.942 ± 0.084, r 2 = 0.926, p < 0.0001 ). (D) Whereas larger torso mass is accompanied by larger numbers of cortical neurons in all early mammalian clades examined, larger carnivorans do not have ever growing numbers of cortical neurons. The leo and striped hyena have merely arsenic many cortical neurons as the average frump, which is only slenderly more neurons than the raccoon, and the brown give birth has evening fewer cortical neurons, about a many as found in the cat-o’-nine-tails. (E) The aggregate of the cerebellum scales as a power affair of consistency mass with exponent 0.606 ± 0.042 across carnivorans ( r 2 = 0.972, p < 0.0001, n = 8, plotted ), which is indistinguishable from even-toed ungulate ( exponent, 0.612 ± 0.105, r 2 = 0.944, p = 0.0282, n = 4 ), but lower than the advocate of 0.739 ± 0.074 ( r 2 = 0.900, p < 0.0001, n = 12 ) that applies to primates. (F) The issue of neurons in the cerebellum scales as a ability function of body mass with advocate 0.522 ± 0.056 ( r 2 = 0.935, p < 0.0001, n = 8, plotted ), which overlaps with the baron functions that apply to other clades except for primates ( exponent, 0.754 ± 0.073, r 2 = 0.906, p < 0.0001, n = 13 ) and for eulipotyphlans ( exponent, 0.873 ± 0.088, r 2 = 0.970, p = 0.0022, n = 5 ). (G) The mass of the rest of mind of carnivoran species scales as a exponent routine of body aggregate with advocate 0.540 ± 0.035 ( r 2 = 0.976, p < 0.0001, n = 8, plotted ), which overlaps with the office functions that apply to early clades except for primates ( exponent, 0.706 ± 0.076, r 2 = 0.896, p < 0.0001, n = 12 ). (H) The number of neurons in the rest of brain of carnivoran species scales as a ability function of body mass with exponent 0.269 ± 0.042 ( r 2 = 0.872, p = 0.0007, n = 8 ), or 0.282 ± 0.028 without the raccoon ( r 2 = 0.953, p = 0.0002, n = 7, plotted ), which has more neurons in the rest of genius than expected for consistency mass. Although the beginning advocate is not importantly different from the exponent that applies to artiodactyls ( r 2 = 0.227 ± 0.027, r 2 = 0.973, p = 0.0136, n = 4 ), carnivoran species seem to have fewer neurons in the pillow of brain than even-toed ungulate of similar body mass ( unfilled circles ) .

Within the mind, carnivorans have cerebellum of comparable mass and numbers of neurons to other non-primate mammals of similar body mass, even-toed ungulate in particular ( Figures 3E, F ). interestingly, the rest of brain is reasonably smaller in aggregate in carnivorans compared to artiodactyls of like body mass ( Figure 3G ), and besides has significantly fewer neurons in carnivorans compared to artiodactyls and actually respective other non-primate mammalian species of like body mass ( Figure 3H ). The raccoon, however, appears to have more neurons in the pillow of genius than predicted for its consistency mass ; indeed, removing the raccoon from the analysis improves the match of the function that describes how the number of neurons in the RoB scales with soundbox aggregate across carnivoran species ( Figure 3H ) .
As found in early mammalian clades, larger carnivoran species have larger cerebral cortices, whose mass is comparable to that of even-toed ungulate and respective early non-primate mammal species of alike consistency mass ( Figure 3C ). strikingly, however, larger carnivorans do not have increasingly more neurons in the cerebral lens cortex. While ferret, mongoose and cat have increasingly larger cortices ( 3.1 gigabyte, 9.3 g, and 24.2 g ) with increasingly more neurons ( 39 million, 116 million, and 250 million neurons, respectively ), we find that the lion has approximately as many neurons in the cerebral lens cortex as the average found in dogs, ca. 500 million neurons, despite a twice larger cortex in the lion than in the dogs ( 139.9 thousand vs. 65.5 gigabyte ; Table 1 ). even more strikingly, the brown bear has fewer neurons in the cerebral cerebral cortex than these two species, 251 million neurons, which is only about a many as the firm kat, tied though the brown have a bun in the oven cortex had a closely 10-fold larger bulk of 222.0 g ( Figure 3D and Table 1 ). The raccoon besides stands out in its number of cortical neurons, but in a different direction : although the mass of the cerebral lens cortex in both raccoon and big cat is a alike 24 gravitational constant, the raccoon cerebral cortex has an average 438 million neurons compared to 250 million neurons in the vomit ( mesa 1 ). signally, of all the individuals we analyzed, the matchless with the most neurons in the cerebral lens cortex was a golden retriever dog ( 627 million neurons ), followed by the lion ( 545 million neurons ), one of the raccoons ( 512 million neurons ), the clean hyena ( 495 million neurons ), a smaller chase of unspecified breed ( 429 million neurons ) and a second raccoon individual ( 395 million neurons ). As a resultant role, the relationship between numbers of cerebral cortical neurons and body mass in carnivorans seems to saturate around 500–600 million neurons, and possibly adopt the condition of an anatropous uranium with lone half as many neurons in the brown university bear cerebral cerebral cortex ( Figure 3D ), a traffic pattern that has not been observed in any other mammal clade sol far, where simple might laws apply ( Herculano-Houzel et al., 2014b ) .
In line with the smaller numbers of cortical neurons than expected for the batch of the cerebral lens cortex in the largest carnivorans examined, we find that while the banded mongoose, big cat, frank and hyena adjust to the scale relationship between cerebral cortical aggregate and numbers of cortical neurons that applies to non-primate mammals ( Figure 4A, plotted function ), the leo has fewer neurons in its cerebral cortex than expected for its cortical bulk ( although still within the 95 % confidence interval for individual values ), and the brown digest falls well outside the 95 % confidence time interval for that kinship, with about aaa the number of neurons predicted for its cortical multitude ( Figure 4A, black ). The ferret besides has fewer neurons in the cerebral cerebral cortex than expected for a non-primate, although airless to the 95 % confidence interval ( Figure 4A, green ). In contrast, the raccoon has more neurons in its cerebral lens cortex than expected for a non-primate mammal of its cortical bulk, approaching the kinship expected for a archpriest ( Figure 4A, crimson circle and triangles ). indeed, while the ring mongoose, caterpillar, frump and hyena have neural densities in the cerebral cortex that decrease predictably with increasing numbers of cortical neurons according to the scaling relationship that applies to early non-primates ( Figure 4B ), the raccoon has an average neural concentration in the cerebral cerebral cortex that is about three times the expected for a non-primate mammal with its number of neurons in the cerebral cerebral cortex, approaching neural densities found in primate cortices. On the other hand, neural densities are respective times smaller than expected in the ferret, lion and particularly the brown bear cerebral lens cortex for their numbers of cortical neurons, compared to non-primate mammals ( Figure 4B ) .

FIGURE 4

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FIGURE 4. Scaling of mass of brain structures with numbers of neurons in carnivorans. Carnivoran species analyzed in this study are shown in colors according to the key in the graph ; non-carnivoran species are depicted in gray ( primates in triangles, even-toed ungulate as unfilled circles ). Plotted functions apply to the species indicated for each graph and include the 95 % confidence interval for individual values. (A) With the exception of the brown give birth, ferret and raccoon, carnivoran species conform to the might routine that describes how the mass of the cerebral cerebral cortex scales as a baron affair of the act of cortical neurons with exponent 1.588 ± 0.042 across non-primate, non-carnivoran species ( r 2 = 0.978, p < 0.0001, n = 35, plotted ). The function calculated for carnivorans ( without the wear and raccoon ) has an advocate of 1.311 ± 0.136 ( r 2 = 0.959, p = 0.0006, n = 6 ). (B) Again, with the exception of the embrown hold, black-footed ferret and raccoon, the concentration of neurons in the cerebral lens cortex of carnivoran species conforms to the exponent function that describes the scale of neural concentration with the act of cortical neurons of advocate –0.590 ± 0.040 across non-primate, non-carnivoran species ( r 2 = 0.865, p < 0.0001, n = 35, plotted ). (C) With the exception of the raccoon, carnivoran species conform to the world power function that describes how the mass of the cerebellum scales as a power function of the number of cerebellar neurons with exponent 1.283 ± 0.035 across the corps de ballet of afrotherians ( minus the African elephant ), even-toed ungulate and glires ( r 2 = 0.987, p < 0.0001, n = 20, plotted ). (D) With the exception of the raccoon, the concentration of neurons in the cerebellum of carnivoran species conforms to the ability function that describes the scaling of neural concentration with the number of cerebellar neurons of advocate –0.283 ± 0.035 across the ensemble of afrotherians ( minus the African elephant ), even-toed ungulate and glires ( r 2 = 0.784, p < 0.0001, n = 20, plotted ). however, the baron function calculated for carnivoran species ( minus the raccoon ) fails to reach meaning ( p = 0.2918 ). (E) The ability function that describes how the mass of the rest of brain scales with the number of rest of brain neurons across even-toed ungulate ( minus the giraffe ), eulipotyphlans and marsupials ( exponent, 2.041 ± 0.143, r 2 = 0.928, p < 0.0001 ; plotted ) includes carnivoran species. (F) Carnivorans are aligned with the scale of neural concentration in the rest of mind with the number of rest of brain neurons that applies to the ensemble of even-toed ungulate ( minus the giraffe ), eulipotyphlans and marsupials, with exponent –1.040 ± 0.142 ( r 2 = 0.769, p < 0.0001, n = 18, plotted ) .

In contrast to the cerebral cortex, the cerebellum of all carnivorans in the dataset conforms to the neural scale rule that applies to the ensemble of afrotherians ( minus the elephant ), glires, and artiodactyls – with the sole exception, again, of the raccoon ( Figure 4C ). The relationship between cerebellar mass and number of cerebellar neurons of carnivorans ( excluding the raccoon ) can be described by a power law of exponent 1.100 ± 0.084 ( r 2 = 0.971, p < 0.0001 ) that is not significantly different from one-dimensionality but is significantly different from the advocate of 1.283 ± 0.035 that applies to the ensemble of afrotherians ( minus the elephant ), glires and even-toed ungulate, which we have proposed to represent the ancestral neural scale rule for the mammalian cerebellum ( Herculano-Houzel et al., 2014b ). In contrast, the raccoon cerebellum has closely two times more neurons than predicted for a mammalian species belonging to those non-primate orders, conforming alternatively to the count of neurons found in the cerebellum of a primate of like cerebellar mass. As expected from these relationships, neural densities in the cerebellum of carnivorans, again with the exception of the raccoon, adjust to the relationship that applies to the ensemble of afrotherians ( minus the elephant ), glires and even-toed ungulate ( Figure 4D ), even though the power function relating neural densities in the cerebellum of carnivorans to the count of neurons in the cerebellum does not reach significance ( p = 0.2918 without the raccoon ; Figure 4D ) .
The mass of the carnivoran rest of brain scales with the count of neurons in the structure raised to an exponent of 1.875 ± 0.134 ( without the raccoon ). This exponent is not significantly different from the exponent of 2.041 ± 0.143 that applies to the ensemble of even-toed ungulate, marsupials and eulipotyphlans ( r 2 = 0.928, p < 0.0001 ; Figure 4E ; Herculano-Houzel, 2017 ), and indeed the 95 % confidence interval for carnivorans includes these species ( Figure 4E ). Rodents, afrotherians and primates depart from this relationship ( Figure 4E ). Carnivoran species adjust to the kinship that describes how neural density in the RoB decreases with increasing number of neurons in the RoB across even-toed ungulate, eulipotyphlans and marsupials ( Figure 4F ) .

Other Cells

The discrepancies between expected and note numbers of neurons in some carnivoran species, most notably the embrown bear, could in principle be due to aberrant immunoreactivity to NeuN, which might fail to label all neurons in these species. similarly, the aberrantly big numbers of neurons found in raccoon mind structures might in principle be due to non-specific label of non-neuronal cells with the anti-NeuN antibody. In these scenarios, any unlabeled neurons in the yield cerebral cortex would be classified as non-neuronal cells and cause aberrantly high numbers of non-neuronal cells in mind structures for their multitude ; conversely, any label glial cells would be mistakenly classified as neurons and lead to aberrantly low numbers of non-neuronal cells in raccoon brain structures. These aberrations would be particularly easy to spot since all major mind structures ( cerebral cerebral cortex, cerebellum and rest of brain ) of all mammalian species examined so far exhibit a relationship between structure mass and number of early ( non-neuronal ) cells that can be described by a one power function of near-linear advocate 1.051 ± 0.014 ( r 2 = 0.974, p < 0.0001 ; Figure 5A ; Herculano-Houzel, 2017 ) . FIGURE 5 www.frontiersin.org
FIGURE 5. All carnivoran species and brain structures conform to the scaling of brain structure mass with numbers of other cells that applies universally across other mammalian species. Cerebral cerebral cortex is shown in circles, cerebellum in squares, pillow of genius in triangles. (A) Brain social organization aggregate scales universally as a power affair of the count of non-neuronal ( other ) cells in the structures across non-carnivoran species ( plat serve ; exponent 1.051 ± 0.014, r 2 = 0.974, p < 0.0001 ), and all carnivorans conform to that relationship. (B) The concentration of other cells in the different structures of carnivoran brains overlaps with densities in the same structures in early mammalian species, which scales very lento as a power function of structure mass of advocate -0.075 ± 0.012 ( r 2 = 0.200, p < 0.0001 ). (C) The proportion between numbers of other cells ( which approximates the number of glial cells ) and numbers of neurons in each structure is not a universal function of structure mass across mammalian species and structures. (D) The proportion between numbers of early cells and neurons in each structure does change universally with average neural density in the social organization across non-carnivoran species ( diagram serve, advocate -0.942 ± 0.019, r 2 = 0.946, p < 0.0001, n = 146 ), and all carnivoran species and brain structures conform to that relationship .

rather, we find that all carnivoran species and brain structures analyzed adjust to the relationship that applies to all early mammalian species, including all raccoon brain structures and the brown university behave cerebral lens cortex ( Figures 5A, B, colored points ). The accord of carnivoran data to the relationship that applies to all other mammalian species and brain structures confirms the universality of the non-neuronal scale rules ( Herculano-Houzel, 2014 ; Mota and Herculano-Houzel, 2014 ). This ossification besides makes it highly improbable that the unexpectedly small ( or big ) numbers of neurons in the brown university give birth cerebral cerebral cortex ( or raccoon mind structures ) are due to misclassification of cells as neurons .
As shown before ( Herculano-Houzel, 2014 ), the ratio between numbers of other cells and neurons is not a universal function of structure mass across mammalian species, including carnivorans ( Figure 5C ). however, this proportion does scale universally with neural density in the structure across all mammalian species analyzed so far, and all carnivorans studied here, including the raccoon and embrown digest, adjust to that same kinship ( Figure 5D ) .

Domesticated vs. Wild Species

The dogs and cat individuals analyzed in this study were domesticated animals, raised by families who donated the brains after the animals died of lifelike causes, in contrast to early animals that were either wild-caught ( raccoon, hyena ) or kept in enslavement ( which might lead to larger torso mass, but are expected to be spokesperson of hazardous species ). notably, we find that these domesticated animals do not deviate from the kinship between brain aggregate ( or issue of neurons ) and body multitude that applies to carnivorans or to non-primates as a whole ( Figure 3 ). additionally, caterpillar and frank data points conform to the relationships between brain social organization aggregate and issue of neurons in the structure that apply to early carnivoran deoxyadenosine monophosphate well as assorted non-primate clades ( see Figure 4 ). Both andiron individuals examined ( a 7.45 kilogram mixed-breed and a 32 kilogram golden retriever ) had larger brains than the vomit ( brain mass in dogs, 58.4 and 114.5 thousand, respectively ; kat, 34.8 thousand ), and besides more mind neurons than the kat ( dogs, 1.8 and 2.6 billion neurons, respectively ; caterpillar, 1.2 billion neurons ). The lapp applies to the cerebral cerebral cortex of the dogs, at 46.2 gram with 429 million neurons and 84.8 deoxyguanosine monophosphate with 623 million neurons, against 24.2 thousand with 250 million neurons in the cat. strikingly, although the cerebral cerebral cortex of the aureate retriever was about doubly equally large as the lens cortex of the smaller dog, it merely had 46 % more neurons than the smaller chase cerebral cortex ( as expected from the non-linear scale of cortical batch with number of cortical neurons, Figure 4 ) ; if plotted individually, both individuals conform to the scale rules that apply to carnivoran species shown in Figure 4, and as expected from their larger cortical mass, both dogs had more neurons in the cerebral cerebral cortex than the computerized tomography. frankincense, the two most common species of domesticate carnivorans do not deviate from the relationship between cortical mass and total of neurons that applies both to wild carnivorans and other non-primate species of exchangeable body, brain or cerebral cortical mass .

Distribution of Cortical Neurons into Cortical Surface Area and Thickness

The apparently decrease number of neurons in the cerebral cortex of large carnivorans for their cortical and torso mass, notably in the embrown hold, could in principle be the resultant role of alter growth that led to the generation of smaller numbers of much larger neurons, resulting in the watch lower neural densities but expected non-neuronal densities. In that case, we might expect the cortical volume to even be distributed into surface area and thickness following the same scale kinship that applies to other carnivorans, with larger surface areas accompanied by slowly increasing cortical thickness. alternatively, if the unexpectedly belittled number of neurons in the cerebral lens cortex of large carnivorans is due to regressive phenomenon after the cortex develops, such as marked neural loss after cortical expansion, we should find evidence of atrophy in the cerebral cerebral cortex of these species, with cortical thinning for their airfoil area, and possibly besides a compact lens cortex for their numbers of cortical neurons ( in case the maximal attained thickness is not wholly lost ), compared to the allometric scaling that applies to other carnivoran species ( but silent the lapp expected non-neuronal densities ). We frankincense determined how the cortical volume was distributed into surface area and thickness across carnivoran species, and how that distribution related to numbers of cortical neurons .
We find that carnivoran cerebral cortices with larger open areas are besides thick, although cortical thickness increases more lento than surface area, as a power function of open sphere with advocate 0.262 ± 0.021 across carnivoran species ( excluding the brown bear ; Figure 6A ). While the raccoon and lion have combinations of cortical airfoil area and thickness that match the prediction for carnivoran species, the brown bear is a open outlier, with a cortical thickness that is excessively small for its coat area, suggestive of cortical atrophy ( thinning ) .

FIGURE 6

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FIGURE 6. Scaling of cortical surface area and thickness with count of neurons in carnivorans. Each carnivoran species is shown in a unlike color according to the keystone in the graph. All other mammals are depicted in grey ( light grey filled circles, glires ; ignite grey unfilled circles, even-toed ungulate ; night gray filled circles, marsupials ; night grey unfilled circles, afrotherians ; filled triangles, primates ; white triangle, scandentia ). For the sake of clearness, scaling relationships for non-carnivoran clades are not plotted. (A) average cortical thickness scales as a exponent affair of cortical surface area with exponent 0.262 ± 0.021 ( r 2 = 0.969, p < 0.0001, n = 7, excluding the brown bear ; plotted in red ; excluding further the raccoon does not change the exponent, which remains 0.262 ± 0.022, p = 0.0003 ). The brown hold has a much thinner cortex for its surface sphere compared to other carnivoran species ; the raccoon, in contrast, has the predicted combination of cortical open area and thickness for a carnivoran. (B) average cortical thickness scales as a power function of the number of cortical neurons with exponent 0.259 ± 0.031 ( r 2 = 0.945, p = 0.0011, n = 6, excluding the brown yield and raccoon ; plotted in red ). (C) cortical surface area scales as a world power affair of the act of cortical neurons with exponent 0.978 ± 0.115, indistinguishable from one-dimensionality ( r 2 = 0.948, p = 0.0010, n = 6, excluding the brown digest and raccoon, plotted in bolshevik ). All values refer to a individual cortical hemisphere .

The distribution of cortical neurons into surface area and thickness besides suggest that a regressive phenomenon is in place. Both the brown yield and lion cortices are thicker than expected for the number of neurons in the cerebral lens cortex ( Figure 6B, total darkness ), consistent with cortices that had more neurons in early development, attained adult-like morphology, but then lost significant numbers of neurons ( and along with them, lost separate of the width of the parenchyma, but not all of it ). similarly, the open sphere of the embrown bear cerebral lens cortex is about one ordain of order of magnitude larger than expected for its number of neurons ( Figure 6C, black ). This radiation pattern is consistent with a reduction in count of neurons in the cerebral cerebral cortex that occurred after cortical expansion in development, when the genius attained its adult density of non-neuronal cells, volume and open sphere, leading to fond thin of the cerebral lens cortex but very little loss of surface sphere .
In contrast to the wear, the raccoon has many more neurons than predicted for a carnivoran species with either its cortical thickness ( Figure 6B, crimson ) or its cortical surface sphere ( Figure 6C, loss ), evening though its cortical thickness x coat area relationship conforms to the pattern that applies to early carnivoran species ( excluding the brown bear ; Figure 6A ). The larger than expected numeral of cortical neurons in the presence of the clade-typical kinship between cortical thickness and surface sphere is consistent with the genesis of larger numbers of smaller neurons ( and therefore the detect increase in neural concentration ) in the raccoon cerebral cerebral cortex, and possibly in the raccoon brain as a whole ( Figure 4 ) .

Scaling across Structures

We have previously found that a one office function indistinguishable from one-dimensionality and with a slope of around 4.0 describes the kinship between numbers of neurons in the cerebellum and in the cerebral lens cortex across all mammal species so far, with the exception of the elephant, which has 44.8 neurons in the cerebellum for every nerve cell in the cerebral lens cortex ( Herculano-Houzel et al., 2014a ). Most carnivorans analyzed adjust to the like relationship that applies to other mammals, with the clean exception of the embrown bear, which, like the elephant, has a much larger ratio between numbers of neurons in the cerebellum and in the cerebral cortex of 36.9 ( trope 7A, black ). unusually, the lion and hyena besides have fewer neurons in the cerebral lens cortex than expected for their number of neurons in the cerebellum, with 7.4 and 6.7 neurons in the cerebellum for every nerve cell in the cerebral cerebral cortex, in contrast to ratios of 3.8 in the cat and raccoon, 3.2 in the pawl and 2.7 in the banded mongoose ( table 1 ) .

FIGURE 7

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FIGURE 7. Scaling of numbers of neurons across genius structures in carnivorans. (A) Except for the brown bear, carnivorans conform to the relationship between numbers of neurons in the cerebellum and in the cerebral cortex that apply to all mammal species examined so far, including primates, but excluding the african elephant ( exponent, 0.928 ± 0.039, indistinguishable from integrity ; r 2 = 0.929, p < 0.0001, plotted ). (B) lone the ferret and brown bear adjust to the scale relationship that describes how the number of neurons in the cerebral cortex varies as a power function of the number of neurons in the perch of brain across glires, eulipotyphlans, and small Afrotherians, with exponent 1.085 ± 0.064, indistinguishable from one-dimensionality ( excluding the African elephant ; r 2 = 0.940, p < 0.0001, n = 20, plotted ). All early carnivoran species, like primates, even-toed ungulate and australasian marsupials, have more neurons in the cerebral cerebral cortex than predicted for the numeral of neurons in the pillow of genius for glires, eulipotyphlans and small Afrotherians. (C) only the banded mongoose among carnivoran species conforms to the scaling kinship that describes how the number of neurons in the cerebellum varies as a power function of the number of neurons in the rest of brain across glires, eulipotyphlans, and belittled Afrotherians, with advocate 1.170 ± 0.119, indistinguishable from one-dimensionality ( excluding the African elephant ; r 2 = 0.842, p < 0.0001, n = 20, plotted ) .

Whereas the cerebral cortex and cerebellum profit neurons proportionately across the huge majority of mammalian species, a alike concerted scaling on numbers of neurons in the cerebral cortex and remainder of genius, with a constant proportion across structures, is true alone across glires, eulipotyphlans, minor afrotherians, and South american marsupials ( Herculano-Houzel, 2016 ). Across these species, a ratio of 2:1 is maintained between neurons in the cerebral cerebral cortex : rest of brain, in what we have proposed to be the ancestral allocation of neurons across these structures ( Herculano-Houzel et al., 2014b ; Herculano-Houzel, 2016 ; Dos Santos et al., 2017 ). Artiodactyls, primates and australasian marsupials deviate from this kinship, with larger ratios between numbers of neurons in the cerebral cerebral cortex and in the rest of brain that may besides increase with brain size. We find that among carnivorans, entirely the ferret out and the brown bear align themselves with the first base group ( Figure 7B ), with small ratios of 2.7 and 3.1 between numbers of neurons in the cerebral lens cortex and the rest of brain, respectively, while all other carnivoran species analyzed align with the moment group that includes primates and artiodactyls, with larger ratios of 5.1 ( mongoose ) to 9-11 ( raccoon, frump and cat-o’-nine-tails ) .
In line with the approximately 4:1 ratio between numbers of neurons in the cerebellum and in the cerebral lens cortex across most species but not the elephant and brown yield, we find that the cerebellum and rest of brain besides gain neurons proportionately across glires, eulipotyphlans, small afrotherians, and South american marsupials, maintaining a ratio of about 8:1 ( Figure 7C ). In contrast, even-toed ungulate, primates and australasian marsupials gain neurons in the cerebellum faster than in the rest of brain ( Figure 7C ). Carnivorans again align with the latter mammal species, with faster addition of neurons to the cerebellum than to the pillow of brain, and thus larger ratios between numbers of neurons in the two structures, compared to glires, eulipotyphlans, and small afrotherians ( Figure 7C ) .

Discussion

here we find that all carnivoran species examined match the relationship between brain structure batch and number of non-neuronal cells that has been found to apply to all mammalian species examined so far ( Dos Santos et al., 2017 ; Herculano-Houzel, 2017 ). This relationship is a consequence of the miss of systematic mutant in the density of non-neuronal cells across brain structures and species. consequently, none of the eight carnivoran species analyzed deviated significantly from the non-neuronal cell densities found previously in other mammal species. These findings are consistent with our proposition that the mechanisms that regulate summation of non-neuronal cells to brain weave have been signally conserved in evolution, which indicates that modal size of non-neuronal cells is tightly controlled in development and does not accept much variation across species or structures ( Mota and Herculano-Houzel, 2014 ). The addition of non-neuronal cells in development with relatively static cell density across brain structures and species seems to besides apply to the raccoon and the brown university hold, regardless of the mechanisms that lead to their deviate neural densities .
Most of the carnivoran species analyzed besides conformed to the relationship between numbers of neurons and neural density found to apply to other non-primate species, and thus besides to the resulting relationship between numbers of neurons and structure mass ( Herculano-Houzel et al., 2014b ; Herculano-Houzel, 2017 ). however, the smallest ( ferret ) and largest ( brown bear ) species had fewer neurons in the cerebral lens cortex than expected for the mass of this structure in a non-primate mammal, a vogue followed besides by the leo, which has a lens cortex with fewer neurons than the gold retriever despite being closely doubly larger. As discourse below, in the context of metabolic cost and the relationships across cortical surface area, thickness and count of neurons, the lower than expected neural densities restricted to the cerebral cortex are indicative of neural loss. conversely, the raccoon had systematically larger neural densities than expected in all three structures examined – cerebral cortex, cerebellum and rest of brain. In the context of a relationship between cortical coat area and thickness that still matched that found for most other carnivoran species, this finding suggests that the raccoon brain develops with a larger number of smaller neurons than expected for a carnivoran, resulting in larger numbers of neurons than expected for a non-primate, approaching the numbers found in archpriest species. indeed, given alone the relationship between brain social organization mass and numbers of neurons, one might unwittingly take the raccoon for a archpriest .

Domestication

Comparisons of the brain aggregate vs. body bulk kinship between domesticated and wild species frequently yield parallel lines with identical slopes, which have been interpreted as decrease brain size in domesticate animals – that is, a downward switch in the relationship ( Kruska, 2007 ). One should keep in mind, however, that a lateral pass shift in the relationship is evenly possible, with tameness inducing larger soundbox masses rather than decreased brain aggregate ( which would be expected due to greater food handiness in captivity ). indeed, recent testify suggests that tameness of the wimp has led by and large to a larger body mass, and to a lesser extent, to larger ( not smaller ) absolute brain mass, chiefly due to enlargement of the cerebellum ( Henriksen et al., 2016 ). Untangling the two possibilities – increased body mass for the size of the brain or decrease brain mass for the size of the body – is not feasible when brain size and consistency size are the merely variables available, and when merely one species is considered in its wilderness and domestic versions. By bringing in other variables and examining other carnivoran angstrom well as other non-primate species, hera we show that laboratory-raised ferrets ampere well as the most common domesticate species, cat and dog, do not have smaller brains or fewer neurons than expected for their body mass. similarly, we have found that the pig shares a relationship between brain aggregate and number of neurons with other artiodactyl and non-primate species, although it is an outlier in its a lot larger consistency batch for its count of brain neurons ( Kazu et al., 2014 ). We therefore have no cause to believe that domesticated animals have become any different from early carnivorans in the allometric scale of their brains ( although the ferret, the smallest carnivoran species examined, might be affected by energetic constraints because of its size ; see below ) .
Intraspecific variation is an important issue to consider in this context. We know that it can be large evening in species considered to be fairly homogeneous such as the testing ground mouse, in which body mass placid varies across young adult animals of same sex and historic period by a agent of 2, and brain mass varies by a gene of 1.33 ( Herculano-Houzel et al., 2015a ). importantly, we found that larger mice do not have significantly larger brains than smaller mouse, and those mouse individuals with larger brains or brain structures do not necessarily have more neurons than individuals with smaller brains or brain structures ( Herculano-Houzel et al., 2015a ). The miss of a strong correlation across individuals mirroring the exponent functions that apply across species can be attributed to the find that across mouse individuals, those with more neurons in a brain structure besides have smaller, not bigger, neurons. This discrepancy suggests a fundamental difference between developmental and evolutionary patterns of brain variation ( Herculano-Houzel et al., 2015a ). indeed, it is well established that allometric relationships that apply across species normally do not apply within species, at least not with the lapp exponents ( Armstrong, 1990 ). The lack of continuity between intra- and interspecies comparisons might distillery be simply ascribable to the typically a lot smaller range of magnetic declination across individuals of a given species, precluding the calculation of accurate relationships – although that should be possible to compensate for with larger sample distribution sizes. Dogs, with their enormous variation in torso and brain size ( at least 15-fold and 2-fold, respectively ; Wosinski et al., 1996 ), offer a capital opportunity to put to test how brain scaling compares within and across species. While we found that the two dog individuals examined did fit the scale relationships observed for other carnivoran species, and indeed for many non-primate mammal species, we couldn ’ triiodothyronine aim to address the issue of how intraspecies scale compares to interspecific scaling hera due to the difficulty of obtaining big numbers of individuals for a proper analyze of intraspecies pas seul .
For all other species, one might be concerned that, except for the raccoon and ferret ( n = 2 for each ), we could lone examine a individual individual. While we acknowledge that intraspecies variation not entirely is meaning but besides is a identical interesting subject in its own right, we still expect it to be negligible when compared to the variation over 2 orders of magnitude in body mass across carnivoran species that we examine here. frankincense, while expanding the analysis to a larger number of individuals of each species would of path have been ideal, we believe it is reasonable to expect that individual magnetic declination in most species other than the dog is improbable to affect the results we report here .

Cognitive Implications

We and others have suggested that the absolute number of neurons in the cerebral cerebral cortex are a major deciding of the cognitive capabilities of different species ( Roth and Dicke, 2005 ; Herculano-Houzel et al., 2014a ; Herculano-Houzel, 2017 ). Testing that prediction requires data on cognitive operation that can be compared across species. It is only recently that data obtained with systematic comparative analyses have started to become available, although most studies continue to focus on finical clades, largely primates ( Deaner et al., 2007 ; MacLean et al., 2014 ; Kabadayi et al., 2016 ) and birds ( MacLean et al., 2014 ; Kabadayi et al., 2016 ). cognitive performance in carnivorans was recently addressed specifically by Benson-Amram et aluminum. ( 2015 ). Across these species, even though brain size relative to body mass is a significant predictor of success in opening a puzzle box, species with larger absolute brain volumes besides tended to be better than others at opening the puzzle box ( Benson-Amram et al., 2015 ). other studies found that absolute brain size ( or absolute size of the cerebral cerebral cortex ) across primates is a much better correlate of tax performance than encephalization quotient ( Deaner et al., 2007 ; MacLean et al., 2014 ). Given that larger archpriest brains are composed of increasing numbers of neurons ( Herculano-Houzel et al., 2007 ; Gabi et al., 2010 ), improved performance thus correlates with increase numbers of neurons across species, and possibly across clades adenine well. indeed, small-brained corvids show similar operation to much larger-brained primates ( Kabadayi et al., 2016 ), which can be explained by their similarly big numbers of pallial neurons despite the remainder in brain size ( Herculano-Houzel, 2017 ). It is thus probable that the larger the number of neurons found in the cerebral lens cortex of a carnivoran, the more cognitively able the species is .
The doubly larger absolute total of neurons we find in the cerebral cerebral cortex of the dog compared to the domestic kat suggests that dogs have a cognitive advantage over cats – and raccoons, despite their smaller brain size compared to dogs, should have like capabilities to dogs. unfortunately, no dogs, cats or raccoons were examined in the comprehensive cogitation of carnivorans by Benson-Amram et aluminum. ( 2015 ), nor were cats and raccoons included amongst the few carnivorans studied by MacLean et alabama. ( 2014 ), only dogs. While our finding of larger numbers of cortical neurons in dogs than in cats may confirm anecdotal perceptions of chase owners and animal trainers a well as unpublished reports that dogs are easier to train and therefore “ more healthy ” ( Greene, 2011 ), cat owners would credibly protest, and rightly so. Any argument about their cognitive capabilities at this orient will be largely a matter of opinion until lineal, systematic comparisons of cognitive capacitance are performed across these and other species. furthermore, given that both cats and dogs seem to obey the lapp neural scale rules for the cerebral cerebral cortex, any difference in cognitive capabilities between them due to differences in numbers of cortical neurons would be tied to differences in resulting brain size, suggesting that cat-sized dogs, if they have cat-sized brains, might have alone arsenic many cortical neurons as domestic cats. placid, our data allow us to predict that, with their larger numbers of neurons in the cerebral lens cortex, dogs of the sizes examined here should have more complex and flexible cognition than cats .
It was once believed that dogs had evolved special forms of cognition relative to their barbarian counterparts, wolves ( Frank, 1980 ), but the like writer former concluded that his dissertation was incorrect and no such difference existed ( Frank, 2011 ). That proposition was, however, taken up by other authors, who argued that dogs had evolved forms of “ human-like sociable cognition ” ( Hare et al., 2002 ). however, Wynne ( 2016 ) argues that “ dogs are better viewed as equipped with the same cognitive skills as many other species, but, living in proximity to and much being wholly pendent on homo beings, they acquire exquisite sensitivity to human action ” ( Wynne, 2016 ). Although the domestic kat has been a favored non-primate model for neurophysiological studies of sensory systems and sensing, not much has been done to examine its cognitive capabilities, particularly in address comparison to the domestic frank ( Shreve and Udell, 2015 ). These authors have called care to how popular articles frequently present cat cognition with a negative spin, whereas research suggests that domestic cats, like dogs, have developed a scope of behaviors that facilitate their interaction with humans. This is an issue that can only be solved by calculate comparisons of cognitive capabilities between cats and dogs – though this is only a detail case of how ill needed are taxonomic comparisons of cognition and behavior across species that can be related to quantitative neuroanatomy ( Herculano-Houzel, 2017 ) .
Raccoons have farseeing been considered highly intelligent animals, “ calculating, ” “ curious ” and “ arch, ” and were initially classified as related to the fox, then as species of imp, until being granted their current status as carnivorans ( reviewed in Pettit, 2010 ). Because of their cognitive “ fame, ” raccoons became the focus of respective studies on their behavior in the early days of psychological inquiry in the beginning of the twentieth century ( Pettit, 2010 ). Placing raccoons on a comparative scale with early animals, however, requires direct comparisons of cognitive performance across species that are silent lacking. It is interesting to combine our finding that the raccoon is an outlier in its numbers of neurons in all brain structures compared to other non-primates, with larger, primate-like numbers of neurons alternatively, with the estimate that the raccoon actually has a relatively small prefrontal cerebral cortex in comparison to carnivorans with exchangeable or even smaller brain and consistency sizes ( Arsznov and Sakai, 2013 ). For exercise, the prefrontal lens cortex represents only 10 % of the raccoon mind volume vs. 20 % in the coatimundi, even though the raccoon brain is twice deoxyadenosine monophosphate large as the brain of the coatimundi ( Arsznov and Sakai, 2013 ). It is possible that the large number of cortical neurons and the larger than expected neural density in the raccoon are at least partially related to an expanded somatosensory cerebral cortex ( Welker and Seidenstein, 1959 ; Welker and Campos, 1963 ). We are presently examining how numbers of neurons in the prefrontal area of the cortex compare across raccoons and early species, but our current results suggest that the relatively small size of the raccoon prefrontal lens cortex may be compensated by its by chance high neural density, frankincense resulting in a large absolute issue of prefrontal neurons, careless of an expanded somatosensory cerebral cortex .
Along the same lines, we were initially surprised to find that carnivorans align with even-toed ungulate in the neural scale relationship that applies to their cerebral cortex, such that the leo, a predatorial carnivoran, has only about as many neurons in the cerebral cerebral cortex as big artiodactyl species that this species preys upon. The similarity fails to support the universe of cocksure selective pressure for larger numbers of neurons in predators compared to their prey species, which would presumably be associated with the cognitive requirements of hunting. In this context, however, two possibilities remain that we are now investigating : ( 1 ) that like numbers of neurons are distributed differently in airfoil area and thickness in carnivorans and even-toed ungulate, such that the number of functional cortical areas, and consequently cortical cognitive output, may be strikingly unlike across them ; and ( 2 ) that for similar numbers of cortical neurons, carnivorans have a larger proportion of these neurons, and therefore a larger absolute number of them, in prefrontal, associative regions involved in goal set and planning.

The Largest Carnivoran Cortices Do Not Have the Most Neurons: Evidence of Trade-Off with Body Mass

While being a bombastic carnivoran brings the advantage of not being preyed upon, it comes with a high energetic cost that has been calculated to impose evolutionary constraints on soundbox size in these predators ( Carbone et al., 1999, 2007 ). The large mundane carnivorans are constrained to preying on large species, which have limiting low population densities ( Carbone et al., 1999 ), and are promote limited by raven biomass and productivity ( i.e., prey biomass produced per year ; Carbone and Gittleman, 2002 ). As a result, the largest carnivorans are peculiarly vulnerable to decreases in prey abundance : these lead to a five to six fold greater decrease in population concentration of the largest carnivorans compared to the effect on the population concentration of smaller carnivoran species ( Carbone et al., 2011 ). similarly, carnivorans must hunt for longer in areas of low prey concentration or productivity ( Carbone et al., 2011 ) .
Hunting in itself is metabolically dearly-won, peculiarly when hunting for large prey, which requires high speed chases, as the energetic cost of hunting is proportional to chase accelerate ; as a result, large-prey specialists expend about twice deoxyadenosine monophosphate much energy during hunting as a small-prey specialist of same body bulk would ( Carbone et al., 2007 ). Hunting big prey is indeed costly that there is a limit to the extra hunt effort that large carnivorans can placid afford to make up for eventual dearth or loss of prey to competitors. For example, losing just 25 % of their prey to scavenging hyenas would cause african violent dogs, an average-sized species ( ca. 25 kilogram torso bulk ), to need to increase their casual hunt time from 3.5 h to over 12 h ( Gorman et al., 1998 ). Such an increase which would be physiologically indefensible : because of the high metabolic monetary value of high-speed hunt, African wilderness dogs already require more than five times the bode basal casual energy consumption for a mammal of their torso bulk, which is close to the calculate physiological limit on sustainable metabolic rates of around 6–7 times the basal metabolic rate ( Gorman et al., 1998 ). Because any addition in the time spent hunting greatly adds to overall energy consumption, which offsets the possible gains of extra hunt hours, large predaceous carnivoran species, with already extremely high hunt costs, are peculiarly susceptible to changes in feeding ecology. additionally, the cost of locomotion for the very largest carnivoran species, the leo and pivotal give birth, are 2–3 times higher than expected for mammals of a similar size ( Chassin et al., 1976 ; Hurst et al., 1982 ) .
The brown bear, the largest carnivoran species we analyzed, is omnivorous : this species both eats grass, berries, bulbs and tuber, and hunts. Adding vegetables to their diet, however, is hush not enough to make brown bears invulnerable to food handiness, as their body mass depends on it. For exercise, the largest north american brown university bears occur in populations that feed on abundant spawn salmon, which does not occur in Europe, and european brown bears are larger in the North than in the South, which appears to be related to greater handiness and use of protein-rich kernel and insects in the North ( Swenson et al., 2007 ). Female body aggregate is highly positively correlated with generative success across populations, which besides indicates that obtaining enough calories is of great consequence ( Hildebrand et al., 1999 ) .
Taken together, the energetic costs of being a big carnivoran suggest that balancing their department of energy budgets requires adjustments that reduce energy consumption ( Carbone et al., 2007 ). One such adaptation is behavioral inaction ( in which animals may or may not be asleep ) : lions, for case, spend over 90 % of the day dormant ( Schaller, 1972 ). Another have that minimizes monetary value is hibernation, which is found in bears and lowers metabolism enough that the body is not damaged by the prolong anorexia, to the orient where not even the expected loss in bone density and muscular mass and force from prolong inaction occur in hibernating bears ( Hershey et al., 2008 ; McGee-Lawrence et al., 2009, 2015 ) .
We suggest that the decrease in the count of neurons in the cerebral cortex of the largest species we examined, the brown bear, and possibly in the lion arsenic well, is related to the large metabolic costs of maintaining a big body mass, and where applicable, needing to spend energy hunting to maintain that mass. We have previously shown that the metabolic cost of the mind is proportional to its act of neurons, regardless of brain size, and that neurons in the cerebral cortex cost on average 10 times vitamin a much department of energy as neurons in the cerebellum ( Herculano-Houzel, 2011 ). therefore, cerebral cortical neurons are expected to be both more vulnerable to caloric deficit than other brain neurons, and to besides contribute more to decreasing entire metabolic price when their numbers are reduced than the loss of early neural populations would. In this regard, we interpret the line up of a much larger than expected ratio between numbers of neurons in the cerebellum and in the cerebral cerebral cortex in the brown wear as a consequence of an abnormally decreased total of neurons in its cerebral cerebral cortex, given that the brown university have a bun in the oven has merely slenderly fewer neurons in the cerebellum than expected for its aggregate, but far fewer neurons in the cerebral cerebral cortex than expected for its mass. This is in contrast to the elephant, the only other exception therefore far to the average 4 neurons in the cerebellum to every nerve cell in the cerebral lens cortex, in which the cerebral lens cortex fits the expected relationship between phone number of neurons and structure mass for afrotherians, while the cerebellum has more neurons than expected for its mass ( Herculano-Houzel et al., 2014a ). The discrepancy in the cerebellum alone indicates that the elephant has an hypertrophied number of cerebellar neurons, possibly related to somatosensory and motive march of the luggage compartment ( Herculano-Houzel et al., 2014a ). A reduce number of cortical neurons in the largest carnivoran species might either be a direct developmental response to caloric deficit, or an evolutionarily incorporated strategy of elimination of cortical neurons that occurs in the largest animals, regardless of their individual developmental history. At the moment we can not distinguish between these possibilities, although they are not mutually exclusive .
It is possible that the smaller than expected issue of cortical neurons found in the brown university behave is immediately due to hibernation, preferably than to the metabolic limitation that leads to hibernation. Differentiating between these two possibilities would require determining cellular constitution of the mind in pre- and post-hibernation animals, and in adolescent bears that have never hibernated. however, as mentioned above, the very advantage of hibernation seems to be that metabolism is lowered enough that the body is not damaged by the drawn-out anorexia, and frankincense we find that neural loss during this time period of lower metabolic pace would be improbable, fair as there is no loss in bone density of muscular mass in hibernating bears ( Hershey et al., 2008 ; McGee-Lawrence et al., 2009, 2015 ). furthermore, despite the presumptive thin of the cortical parenchyma, there were no signs of adult ( such as age-related ) cortical atrophy, such as gaps between the gyrus in the embrown wear lens cortex. similarly, we found no signs of neural loss in another hibernating animal we analyzed previously, the gray squirrel, compared to non-hibernating rodent species ( Herculano-Houzel et al., 2011 ) .
Carbone et aluminum. ( 2007 ) have suggested that the daily energetic expending scales differently with body mass between small and big carnivoran species. interestingly, the limit between the two groups is at a soundbox mass of 14.5–21 kilogram, where domestic dogs are found. domestic dogs have adapted to the starch-rich diet that is typical of modern humans ( Axelsson et al., 2013 ), which might protect them from metabolic constraints that apply to early carnivorans. importantly, we find that dogs do not have more cortical neurons than predicted for a non-primate of its cortical multitude, but just a many as expected. It will be interesting to determine if wolves, with a larger brain size than most domestic dogs, besides have angstrom many cortical neurons as predicted, or if there already is evidence that, because of the dependence on hunting, they are subject to a tradeoff between body bulk and number of cortical neurons as the embrown bear and, possibly, the leo .
unusually, at the abject end of the body aggregate scope of carnivorans, small predators such as the ferret are besides expected to face metabolic constraints, due to the dearly-won strategy of feeding on much smaller prey ( Carbone et al., 2007 ). Their higher than expected daily energy expending might therefore impose a tradeoff on the issue of cortical neurons found in the black-footed ferret cerebral cortex, which we have besides found to be lower than expected for the cortical batch of this species, with importantly reduced neural densities. Expanding this survey to a larger numeral of carnivoran species spanning the fully range of consistency masses in the clade will help elucidate whether trade-offs between numbers of cortical neurons and body bulk do happen as a rule in both the upper and lower limits of body size in carnivorans .

Author Contributions

SH-H, DJ-M, and PM designed the research ; KL, SN, MB, FP, MECL, OM, AA, and PM provided tissue ; DJ-M and SH-H collected and analyzed data and wrote the manuscript .

Funding

This work was funded by FAPERJ, CNPq, the James S. McDonnell Foundation, and individual contributions through crowdfunding to SH-H ; generous back through the Schapiro Undergraduate Research Fund at Randolph-Macon College to KL ; the Vice Deanship of Research Chairs at the King Saud University to AA and OM ; and the National Research Foundation of South Africa to PM .

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or fiscal relationships that could be construed as a potential conflict of interest .

Acknowledgments

The authors thank Jon Kaas for comments on the manuscript, Stan Gehrt ( Ohio State University ) for trapping raccoons, Jessica Brito for technical patronize during this discipline, and the generous support of brazilian crowdfunding contributors during the last stages of data collection .

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