Endocranial Development in the Coyote (Canis latrans) and Gray Wolf (Canis lupus): A Computed Tomographic Study.

The purpose of this study was to examine the pattern of postnatal brain growth in two wild canid species: the coyote (Canis latrans) and gray wolf (Canis lupus). Adult regional and total brain volume differences were also compared between the two species as well as within each species by sex. Three-dimensional virtual endocasts of endocranial airspace were created from computed tomography scans of 52 coyote skulls (28 female, 24 male; 1 day to 13.4 years) and 46 gray wolf skulls (25 female, 21 male; 1 day to 7.9 years). Age was known in coyotes or estimated from dentition patterns in wolves. The 95% asymptotic growth of the endocranium is completed by 21 weeks in male and 17.5 weeks in female coyotes and by 27 weeks in male and 18.5 weeks in female wolves. These ages are well before age at first reproduction (coyote - 40.4 weeks; wolf - 91.25 weeks). Skull growth as measured by centroid size lags behind endocranial growth but is also completed before sexual maturity. Intra- and interspecific comparisons of brain volumes in the adult wolves and coyotes revealed that relative anterior cerebrum (AC) volume was greater in males than females in both species. Relative brain size was greater in the coyote than in the wolf as was relative cerebrum volume. However, relative AC volume and relative cerebellum and brainstem volume was greater in the wolf than coyote. One explanation for the increased AC volume in males compared to females may be related to the role of social information processing. However, additional data are needed to determine the correspondence between regional volumes and functional differences either between or within these species. Nonetheless, these findings provide important baseline data for further studies on wild canid brain variations and development.

Big Cat Coalitions: A Comparative Analysis of Regional Brain Volumes in Felidae.

Broad-based species comparisons across mammalian orders suggest a number of factors that might influence the evolution of large brains. However, the relationship between these factors and total and regional brain size remains unclear. This study investigated the relationship between relative brain size and regional brain volumes and sociality in 13 felid species in hopes of revealing relationships that are not detected in more inclusive comparative studies. In addition, a more detailed analysis was conducted of four focal species: lions (Panthera leo), leopards (Panthera pardus), cougars (Puma concolor), and cheetahs (Acinonyx jubatus). These species differ markedly in sociality and behavioral flexibility, factors hypothesized to contribute to increased relative brain size and/or frontal cortex size. Lions are the only truly social species, living in prides. Although cheetahs are largely solitary, males often form small groups. Both leopards and cougars are solitary. Of the four species, leopards exhibit the most behavioral flexibility, readily adapting to changing circumstances. Regional brain volumes were analyzed using computed tomography. Skulls (n = 75) were scanned to create three-dimensional virtual endocasts, and regional brain volumes were measured using either sulcal or bony landmarks obtained from the endocasts or skulls. Phylogenetic least squares regression analyses found that sociality does not correspond with larger relative brain size in these species. However, the sociality/solitary variable significantly predicted anterior cerebrum (AC) volume, a region that includes frontal cortex. This latter finding is despite the fact that the two social species in our sample, lions and cheetahs, possess the largest and smallest relative AC volumes, respectively. Additionally, an ANOVA comparing regional brain volumes in four focal species revealed that lions and leopards, while not significantly different from one another, have relatively larger AC volumes than are found in cheetahs or cougars. Further, female lions possess a significantly larger AC volume than conspecific males; female lion values were also larger than those of the other three species (regardless of sex). These results may reflect greater complexity in a female lion's social world, but additional studies are necessary. These data suggest that within family comparisons may reveal variations not easily detected by broad comparative analyses.

The procyonid social club: comparison of brain volumes in the coatimundi (Nasua nasua, N. narica), kinkajou (Potos flavus), and raccoon (Procyon lotor).

The present study investigated whether increased relative brain size, including regional brain volumes, is related to differing behavioral specializations exhibited by three member species of the family Procyonidae. Procyonid species exhibit continuums of behaviors related to social and physical environmental complexities: the mostly solitary, semiarboreal and highly dexterous raccoons (Procyon lotor); the exclusively arboreal kinkajous (Potos flavus), which live either alone or in small polyandrous family groups, and the social, terrestrial coatimundi (Nasua nasua, N. narica). Computed tomographic (CT) scans of 45 adult skulls including 17 coatimundis (9 male, 8 female), 14 raccoons (7 male, 7 female), and 14 kinkajous (7 male, 7 female) were used to create three-dimensional virtual endocasts. Endocranial volume was positively correlated with two separate measures of body size: skull basal length (r = 0.78, p < 0.01) and basicranial axis length (r = 0.45, p = 0.002). However, relative brain size (total endocranial volume as a function of body size) varied by species depending on which body size measurement (skull basal length or basicranial axis length) was used. Comparisons of relative regional brain volumes revealed that the anterior cerebrum volume consisting mainly of frontal cortex and surface area was significantly larger in the social coatimundi compared to kinkajous and raccoons. The dexterous raccoon had the largest relative posterior cerebrum volume, which includes the somatosensory cortex, in comparison to the other procyonid species studied. The exclusively arboreal kinkajou had the largest relative cerebellum and brain stem volume in comparison to the semi arboreal raccoon and the terrestrial coatimundi. Finally, intraspecific comparisons failed to reveal any sex differences, except in the social coatimundi. Female coatimundis possessed a larger relative frontal cortical volume than males. Social life histories differ in male and female coatimundis but not in either kinkajous or raccoons. This difference may reflect the differing social life histories experienced by females who reside in their natal bands, and forage and engage in antipredator behavior as a group, while males disperse upon reaching adulthood and are usually solitary thereafter. This analysis in the three procyonid species supports the comparative neurology principle that behavioral specializations correspond to an expansion of neural tissue involved in that function.

Multiple determinants of whole and regional brain volume among terrestrial carnivorans.

Mammalian brain volumes vary considerably, even after controlling for body size. Although several hypotheses have been proposed to explain this variation, most research in mammals on the evolution of encephalization has focused on primates, leaving the generality of these explanations uncertain. Furthermore, much research still addresses only one hypothesis at a time, despite the demonstrated importance of considering multiple factors simultaneously. We used phylogenetic comparative methods to investigate simultaneously the importance of several factors previously hypothesized to be important in neural evolution among mammalian carnivores, including social complexity, forelimb use, home range size, diet, life history, phylogeny, and recent evolutionary changes in body size. We also tested hypotheses suggesting roles for these variables in determining the relative volume of four brain regions measured using computed tomography. Our data suggest that, in contrast to brain size in primates, carnivoran brain size may lag behind body size over evolutionary time. Moreover, carnivore species that primarily consume vertebrates have the largest brains. Although we found no support for a role of social complexity in overall encephalization, relative cerebrum volume correlated positively with sociality. Finally, our results support negative relationships among different brain regions after accounting for overall endocranial volume, suggesting that increased size of one brain regions is often accompanied by reduced size in other regions rather than overall brain expansion.

Pride diaries: sex, brain size and sociality in the African lion (Panthera leo) and cougar (Puma concolor).

The purpose of this study was to examine if differences in social life histories correspond to intraspecific variation in total or regional brain volumes in the African lion (Panthera leo) and cougar (Puma concolor). African lions live in gregarious prides usually consisting of related adult females, their dependent offspring, and a coalition of immigrant males. Upon reaching maturity, male lions enter a nomadic and often, solitary phase in their lives, whereas females are mainly philopatric and highly social throughout their lives. In contrast, the social life history does not differ between male and female cougars; both are solitary. Three-dimensional virtual endocasts were created using computed tomography from the skulls of 14 adult African lions (8 male, 6 female) and 14 cougars (7 male, 7 female). Endocranial volume and basal skull length were highly correlated in African lions (r = 0.59, p < 0.05) and in cougars (r = 0.67, p < 0.01). Analyses of total endocranial volume relative to skull length revealed no sex differences in either African lions or cougars. However, relative anterior cerebrum volume comprised primarily of frontal cortex and surface area was significantly greater in female African lions than males, while relative posterior cerebrum volume and surface area was greater in males than females. These differences were specific to the neocortex and were not found in the solitary cougar, suggesting that social life history is linked to sex-specific neocortical patterns in these species. We further hypothesize that increased frontal cortical volume in female lions is related to the need for greater inhibitory control in the presence of a dominant male aggressor.

Virtual endocasts: an application of computed tomography in the study of brain variation among hyenas.

Reliable brain volume measurements are crucial in identifying factors that influence the course of brain evolution. Here, we demonstrate the potential for using virtual endocasts (VEs) to examine inter- and intraspecific variation in brain volume in members of the family Hyaenidae. Total endocranial volume (adjusted for body size) and anterior cerebrum volume (adjusted for endocranial volume) were greater in the spotted hyena, the most gregarious of the species, than in the other hyaenids, all of which are less gregarious. An intraspecific analysis of spotted hyenas revealed that anterior cerebrum volume is significantly larger in males than females, although total endocranial volume does not differ between the sexes. Greater total endocranial and anterior cerebrum volume of spotted hyenas, relative to those of other hyena species, may be related to increased neural processing mediating cognitive demands associated with a complex social life. These data demonstrate that computed tomographic (CT) technology can be used to create VEs in species for which actual brains are rare or unavailable, and suggest that this approach can be applied systematically to explore intra- and interspecies brain variations in studies of brain evolution.

Brain size and social complexity: a computed tomography study in Hyaenidae.

The social brain hypothesis posits that the demands of living in complex social groups require increased neural processing, and that this underlies the expansion of brain areas involved in mediation of complex social behavior. However, much of the support for the social brain hypothesis is derived from comparative studies in primates. If large brains evolved as a result of selection pressures imposed by life within complex societies, as the social brain hypothesis predicts, then gregarious nonprimate species should possess large brains and exhibit comparable expansion of brain areas mediating social behavior. Our purpose here was to test a prediction of the social brain hypothesis-- that increased brain size is related to social complexity --by examining species in the carnivore family Hyaenidae. Hyaenidae contains 4 extant species that span a spectrum of social complexity: the aardwolf (Proteles cristata) is solitary during the nonbreeding season, and forms monogamous pairs during the breeding season; the striped hyena (Hyaena hyaena) lives solitarily or in small groups; the brown hyena (Parahyaena brunnea) lives in groups of up to 14 individuals; and the spotted hyena (Crocuta crocuta) lives in complex hierarchically organized groups containing up to 90 animals. Computed tomography was used to create three-dimensional endocasts based on serial analysis of coronal sections of the adult endocranium. The largest brain volume, relative to body size, is found in the spotted hyena. We found no significant variation in relative brain volume among striped hyenas, brown hyenas, and aardwolves. The spotted hyena also possesses a larger anterior cerebrum volume relative to total brain volume than is found in the other hyena species; this region is composed primarily of frontal cortex. These data are consistent with the idea that expansion of the frontal cortex is driven by the demands of processing cognitive information associated with complex social lives, but other factors may drive the evolution of large brains in hyaenids.

Sex and the frontal cortex: A developmental CT study in the spotted hyena.

The purpose of this study was to examine developmental and individual variation in total endocranial volume and regional brain volumes, including the anterior cerebrum, posterior cerebrum and cerebellum/brain stem, in the spotted hyena (Crocuta crocuta). The spotted hyena is a highly gregarious animal noted for living in large, hierarchically organized groups. The social lives of male and female spotted hyenas do not differ until after puberty, when males disperse from the natal group, while females remain philopatric. Here we sought to determine whether the divergent life histories of male and female spotted hyenas are linked to differences in brain size or organization. Three-dimensional virtual endocasts were created using computed tomography from 46 spotted hyenas skulls (23 females, 22 males, 1 unknown sex) ranging in age from 1 day to 18 years. Brain volume and skull length were highly correlated (r = 0.91), and both reached asymptotic values by 34 months of age. Analyses of total endocranial volume (relative to skull length) and cerebellum/brain stem volume (relative to total endocranial volume) revealed no sex differences. However, relative anterior cerebrum volume, comprised mainly of frontal cortex, was significantly greater in adult males than adult females, and relative posterior cerebrum volume was greater in adult females than adult males. We hypothesize that the demands of neural processing underlying enhanced social cognition required for successful male transfer between matriarchical social groups at dispersal may be greater than cognitive demands on philopatric females.

Social intelligence in the spotted hyena (Crocuta crocuta).

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.

Somatosensory input to the ventrolateral thalamic region in the macaque monkey: potential substrate for parkinsonian tremor.

In the present study, we determined the anatomic relationships between somatosensory and motor pathways within ventrolateral (VL) thalamic nuclei of the motor thalamus of macaque monkeys. In labeling experiments, four macaque monkeys (Macaca mulatta) received injections of biotinylated dextran amine and wheat germ agglutinin conjugated to horseradish peroxidase into the cerebellar nuclei or internal segment of the globus pallidus and cervical segments of the spinal cord, respectively. Each tracer was visualized in brain sections by sequentially using a different chromogen. Labeled terminals were plotted and superimposed on adjacent brain sections processed for Nissl substance, acetylcholinesterase, and the antigens for calbindin and Cat-301 to reveal thalamic nuclei. The labeled cerebellar terminals were distributed throughout the posterior VL (VLp), whereas the labeled pallidothalamic terminals were concentrated in the anterior VL and the ventral anterior nucleus. The spinothalamic input was directed mostly to the ventral posterior complex and cells just caudal to it. In addition, the patches of spinothalamic terminations intermingled and partly overlapped with the cerebellothalamic, but not with the pallidothalamic terminations within VLp. The regions of overlap of somatosensory and cerebellar inputs within the VLp of the present study appear to correspond to the reported locations of the tremor-related cells in parkinsonian patients. Thus, the overlapping spinothalamic and cerebellar inputs may provide a substrate for the altered activity of motor thalamic neurons in such patients.

The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey.

The purpose of the present study was to determine the interrelationship between the thalamic afferents arising from the cerebellum (Cb) and the internal segment of the globus pallidus (GPi) with the neurons projecting to the primary motor cortex (MI) and to the supplementary motor area (SMA). We combined fluorescent retrograde tracers with a double anterograde labeling technique. Multiple injections of a combination of Diamidino Yellow and Fast Blue were made into either the MI or SMA hand/arm representation as determined by intracortical microstimulation. In the same animal, biotinylated dextran amine was injected into the GPi and horseradish peroxidase conjugated to wheat germ agglutinin was injected into the contralateral cerebellar nuclei. The results revealed that the cerebellar and pallidal thalamic territories are largely separate. The ventral anterior nucleus (VA) and the ventral lateral nucleus pars oralis (VLo) contained a greater density of pallidal labeling while a greater density of cerebellar label was observed more caudally in the ventral posterior lateral nucleus pars oralis (VPLo) as well as in nucleus X (X). Moreover, we observed that the greatest coincidence of retrograde cell labeling was within the pallidal thalamic territory following the SMA injections and within the cerebellar thalamic territory following the MI injections. However, interdigitating foci of pallidal and cerebellar label were also observed particularly in the ventral lateral nucleus pars oralis (VLo) and the ventral lateral nucleus pars caudalis (VLc). In both VLo and VLc, we additionally observed coincidence between the cerebellar labeling and SMA projection neurons as well as between pallidal labeling and MI projection neurons. These data suggest that while MI primarily receives inputs originating from Cb and SMA primarily receives inputs originating from GPi, it also appears that MI and SMA receive secondary afferents arising from GPi and Cb, respectively.