Atypical play experiences in the juvenile period has an impact on the development of the medial prefrontal cortex in both male and female rats.

In rats reared without play, or with limited access to play during the juvenile period, the dendrites of pyramidal neurons of the medial prefrontal cortex (mPFC) exhibit more branching than rats reared with more typical levels of play. This suggests that play is critical for pruning the dendritic arbor of these neurons. However, the rearing paradigms typically used to limit play involve physical separation from a peer or sharing a cage with an adult, causing stress that may disrupt pruning. To limit this potentially confounding source of stress, we used an alternative approach in this study: pairing playful Long Evans rats (LE) with low playing Fischer 344 (F344) rats throughout the juvenile period. We then examined the morphology of medial prefrontal cortex (mPFC) neurons, predicting that pruning should be reduced. LE rats reared with another LE rat had significantly greater pruning of mPFC pyramidal neurons compared to LE rats reared with a F344 partner. Furthermore, in previous studies, only one sex or the other was used, whereas in the present rearing paradigm, both sexes were tested, showing that play influences neuronal pruning in both. The neurons of the play deficient LE rats not only occupied more space, as determined by convex hull analyses, but the dendrites were also longer than in rats with more typical play experiences. Unlike studies using more stressful rearing paradigms, the present effects were limited to the apical dendritic projections, suggesting that the previously reported effects on the basilar dendrites may have resulted from developmental disruptions caused by stress. If correct, the present findings indicate that play experienced over the juvenile period affects how mPFC neurons develop and function.

Seasonal differences in the morphology and spine density of hippocampal neurons in wild ground squirrels.

Seasonally reproducing small mammals often undergo changes in brain anatomy throughout the year. Much of the research on this seasonal neuroplasticity has focused on changes in hippocampus volume and neurogenesis, with relatively little attention paid to neuronal morphology. Here, we test for sex, season and sex-season interaction effects on hippocampal neuron morphology and dendritic spine density in a seasonally reproducing rodent: Richardson's ground squirrel (Urocitellus richardsonii). We quantified the morphology and spine densities of Golgi-stained pyramidal neurons and granule cells in the hippocampus and tested for differences between sexes and seasons with generalized linear models. Although we found no significant sex differences or sex-season interaction effects on any of our morphological measurements, there were significant differences in neuron morphology and spine density between breeding and non-breeding seasons. In the non-breeding season, ground squirrels had CA1 neurons with longer basal dendrites with more branches than in the breeding season. Non-breeding season animals also had higher apical and basal dendrite spine density in CA1 and CA3 neurons than breeding-season animals. Conversely, the spine densities of CA1 somata and granule cells were higher in breeding than in non-breeding season. These differences in neuron morphology and spine density between breeding and non-breeding seasons likely arise from a combination of activity levels, stress hormones, and photoperiod. Although the functional implications of seasonal changes in hippocampal neuron morphology and spine density are uncertain, our data suggest that ground squirrels may be a good model for understanding seasonal neuroplasticity in mammals.

The evolution of mammalian brain size.

Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mammalian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.

The size of non-hippocampal brain regions varies by season and sex in Richardson's ground squirrel.

Sex- and season-specific modulation of hippocampal size and function is observed across multiple species, including rodents. Other non-hippocampal-dependent behaviors exhibit season and sex differences, and whether the associated brain regions exhibit similar variation with sex and season remains to be fully characterized. As such, we examined the brains of wild-caught Richardson's ground squirrels (RGS; Urocitellus richardsonii) for seasonal (breeding, non-breeding) and sex differences in the volumes of specific brain areas, including: total brain volume, corpus callosum (CC), anterior commissure (AC), medial prefrontal cortex (mPFC), total neocortex (NC), entorhinal cortex (EC), and superior colliculus (SC). Analyses of variance and covariance revealed significant interactions between season and sex for almost all areas studied, primarily resulting from females captured during the breeding season exhibiting larger volumes than females captured during the non-breeding season. This was observed for volumes of the AC, mPFC, NC, EC, and SC. Where simple main effects of season were observed for males (the NC and the SC), the volume advantage favoured males captured during the NBr season. Only two simple main effects of sex were observed: males captured in the non-breeding season had significantly larger total brain volume than females captured in the non-breeding season, and females captured during the breeding season had larger volumes of the mPFC and EC than males captured in the breeding season. These results indicate that females have more pronounced seasonal differences in brain and brain region sizes. The extent to which seasonal differences in brain region volumes vary with behaviour is unclear, but our data do suggest that seasonal plasticity is not limited to the hippocampus and that RGS is a useful mammalian species for understanding seasonal plasticity in an ecologically relevant context.

The effects of season and sex on dentate gyrus size and neurogenesis in a wild rodent, Richardson's ground squirrel (Urocitellus richardsonii).

Sex and reproductive status affect hippocampal neurogenesis and dentate gyrus (DG) size in rodents. Relatively few studies, however, address these two effects simultaneously and even fewer studies address this issue in wild populations. Here, we examined seasonal and sex differences in neurogenesis and DG size in a wild, polygynous and social rodent, Richardson's ground squirrel (Uriocitellus richardsonii). Based on the behavioral ecology of this species, we predicted that both neurogenesis and DG size would be sexually dimorphic and the degree of dimorphism would be greatest in the breeding season. Using unbiased stereology and doublecortin (DCX) immunohistochemistry, we found that brain volume, DG size and number of DCX cells varied significantly between breeding and non-breeding seasons, but only brain volume and the number of DCX labeled cells differed between the sexes. Both sex and seasonal differences likely reflect circulating hormone levels, but the extent to which these differences relate to space use in this species is unclear. Based on the degree of seasonal differences in neurogenesis and the DG, we suggest that ground squirrels could be considered model species in which to examine hippocampal plasticity in an ecologically valid context.

Sexual selection on brain size in shorebirds (Charadriiformes).

Natural selection is considered a major force shaping brain size evolution in vertebrates, whereas the influence of sexual selection remains controversial. On one hand, sexual selection could promote brain enlargement by enhancing cognitive skills needed to compete for mates. On the other hand, sexual selection could favour brain size reduction due to trade-offs between investing in brain tissue and in sexually selected traits. These opposed predictions are mirrored in contradictory relationships between sexual selection proxies and brain size relative to body size. Here, we report a phylogenetic comparative analysis that highlights potential flaws in interpreting relative brain size-mating system associations as effects of sexual selection on brain size in shorebirds (Charadriiformes), a taxonomic group with an outstanding diversity in breeding systems. Considering many ecological effects, relative brain size was not significantly correlated with testis size. In polyandrous species, however, relative brain sizes of males and females were smaller than in monogamous species, and females had smaller brain size than males. Although these findings are consistent with sexual selection reducing brain size, they could also be due to females deserting parental care, which is a common feature of polyandrous species. Furthermore, our analyses suggested that body size evolved faster than brain size, and thus the evolution of body size may be confounding the effect of the mating system on relative brain size. The brain size-mating system association in shorebirds is thus not only due to sexual selection on brain size but rather, to body size evolution and other multiple simultaneous effects.

Heterogeneity of parvalbumin expression in the avian cerebellar cortex and comparisons with zebrin II.

The cerebellar cortex has a fundamental parasagittal organization that is reflected in the physiological responses of Purkinje cells, afferent and efferent connections, and the expression of several molecular markers. The most thoroughly studied of these molecular markers is zebrin II (ZII; a.k.a. aldolase C). ZII is differentially expressed in Purkinje cells, resulting in a pattern of sagittal stripes of high expression interdigitated with stripes of little or no expression. In this study, we examined the expression of the calcium binding protein parvalbumin (PV) in the cerebellum of several avian species (pigeons, hummingbirds, zebra finches) and compared it to the expression of ZII. We found that PV immunoreactivity was distributed across the cerebellar cortex such that there were sagittal stripes of PV immunopositive (PV+) Purkinje cells alternating with PV immunonegative (PV-) Purkinje cells. Although most Purkinje cells in the anterior lobe were PV+, there were several thin (i.e. only a few Purkinje cells wide) PV- stripes spanning the folia. In the posterior lobe, PV+ and PV- stripes were also apparent, but the PV- stripes were much wider than in the anterior lobe. In sections processed for both ZII and PV, the expression was generally complementary: PV+ stripes were ZII-, and vice-versa. This complementary expression was most apparent in folia II-IV and VIII-IXcd. The complementary expression was not, however, absolute; some Purkinje cells co-expressed PV and ZII whereas others lacked both. These novel findings relate to the complex neurochemical organization of the cerebellum, and are likely important to issues regarding cerebellar plasticity.

A comparative analysis of relative brain size in waterfowl (Anseriformes).

Variation in relative brain size was examined in 55 species of waterfowl (Anseriformes). Using both conventional statistics and phylogenetically based comparative methods, the extent of variation in relative brain size and possible relationships with mode of foraging and diet were examined. The results indicate that although brain size does vary considerably between closely related species of waterfowl, it is not reliably related to either foraging mode or diet. There are a number of possible reasons for the lack of relationships between brain size and foraging mode and diet. Firstly, subtle changes in foraging mode and diet may favor relatively large changes in brain size. Secondly, foraging mode and diet could be correlated with the expansion of an individual brain region without affecting overall brain size. Thirdly, other behavioral/ecological traits may be more important with respect to brain size evolution in waterfowl. For example, the relatively large brain of the musk duck (Biziura lobata) and altriciality of their young in comparison to other stiff-tailed ducks (Oxyura spp.) indicates that developmental rate plays a significant role in the evolution of brain size. Given the difference between our results and that reported in inter-order comparisons of brain size in birds, further research is required into other avian orders to assess how brain size and behavior might be related within orders as well as between them.

Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.

It has been hypothesized that play is more likely to be present in larger brained species. We tested this hypothesis in mammals using independent contrasts, a method that controls for phylogenetic relatedness. Comparisons across 15 orders revealed that the prevalence and complexity of play was significantly correlated with brain size, with larger brained orders having more playful species. Three orders, Rodentia, Marsupialia, and Primates, were used for within-order comparisons among species and, where possible, among families. The comparisons were not significant for rodents or primates, and those for marsupials yielded inconsistent results. Therefore, although a strong relationship is present at the highest taxonomic level of comparison, it diminishes or evaporates at lower level comparisons.

On the origin of skilled forelimb movements.

Homologizing behaviour was once considered unreliable, but the application of modern comparative methods has been shown to provide strong evidence of behavioural homologies. Skilled forelimb movements were thought to originate in the primate lineage but in fact are common among tetrapod taxa and probably share a common origin in early tetrapods. Furthermore, skilled movements are likely to have been derived from, and elaborated through, food-handling behaviour. In addition, it is now thought that the role played by the lateral and medial descending pathways of the spinal cord in the execution of skilled forelimb movements could be synergistic, rather than the exclusive responsibility of an individual pathway.

Comparative analyses of the role of postnatal development on the expression of play fighting.

Whether it is that animals are young so that they can play, or whether it is that they play because they are young, play should be more prevalent in species that have a greater degree of postnatal development. This hypothesis is tested by comparative analyses within two mammalian orders (primates and muroid rodents) using independent contrasts. This technique can account for the relative degree of relatedness among the species. For both orders, the complexity or prevalence of play fighting is compared to the degree of prenatal development (neonatal weight/adult weight). In addition, the prevalence of play in primates is compared to prenatal brain development (neonatal brain weight/adult brain weight). Significant negative regressions show that 30% of the variance in the distribution of play in the rodents is accounted for by the degree of prenatal development of body size, and 60% of the variance in play in the primates is accounted for by prenatal brain growth. The findings are thus consistent with the prediction. Species with a greater proportion of their growth occurring postnatally play more and have more complex play than do species with more of their growth occurring prenatally.

Brain size is not correlated with forelimb dexterity in fissiped carnivores (Carnivora): A comparative test of the principle of proper mass.

To test the hypothesis that brain size and forelimb dexterity are positively correlated, the relative brain size of 41 species of fissiped (terrestrial) carnivores (Order: Carnivora) was examined with respect to their forelimb use during feeding. With the use of a newly derived dexterity index, the forelimb dexterity executed by each of the species was calculated as a single, continuous variable which was then regressed against the residuals of brain size. To account for confounding effects of phylogenetic inertia, the analysis was performed with independent contrasts analysis using a speciational model of evolutionary change (i.e. equal branch lengths). The results suggest that relative brain size and isocortex size are not correlated with the dexterity of the proximal or distal segments or a combination of the two (total forelimb dexterity). The presence of species with widely different brain sizes and similar dexterities, and vice versa, suggests that an increase in the amount of neural substrate might not be necessary for the production of finely coordinated forelimb movements. It is suggested that this outcome is representative of the plasticity of both mammalian brain size and behavior and that variations in brain size and forelimb dexterity could be linked to disparate ecological and phylogenetic factors which act in concert to promote or constrain neural development and behavior in different species.

How skilled are the skilled limb movements of the raccoon (Procyon lotor)?

Raccoons have been widely used for neurobiological research and with respect to paw (hand) use have been 'considered' to be primates because they display highly developed skilled hand use. Their exceptional manipulatory ability is puzzling from an evolutionary perspective both because they belong to a taxon that is divergent from primates and because most members of their taxon are not especially skilled. Surprisingly, there has been no systematic investigation of their manipulatory ability. This was the purpose of the present study. Captive and zoo-housed raccoons were video recorded during food handling in a wide variety of conditions and the video records were subjected to descriptive frame-by-frame analysis aided by the use of Eshkol-Wachman Movement Notation (EWMN). The results confirm that raccoons display good manual skills in food finding, grasping and handling. Like primates, they use vision to identify and reach for objects, but additionally they make extensive use of haptically controlled movements. Unlike primates, they do not have a true convergent hand as it has limited flexive properties. Objects are grasped between the digits or between the apical digit and distal palmar pads. Manipulation of objects consisted of rolling the object between the palms of both hands, with little or no digit movement. Finally, although they can make unimanual reaching movements, they make extensive use of a bimanual reaching strategy. These results suggest that raccoons are like primates in that they display visual guidance of reaching, but are similar to other carnivores in that they do not use convergent grasping and digit manipulation and frequently use bimanual grasping. The results, consistent with a growing body of information on skilled use in mammals, including marsupials and rodents, suggest that raccoons are specialised, but not special.

Is digital dexterity really related to corticospinal projections?: a re-analysis of the Heffner and Masterton data set using modern comparative statistics.

Using a data set of 69 different mammalian species, Heffner and Masterton propose that the longer and deeper the fibres of the corticospinal tract, the greater an animal's digital dexterity. Because of the effects that phylogeny may have upon the extant phenotype of a given species, however, data from a wide range of species can rarely be considered to represent fully independent data points. Using modern comparative statistics, which incorporate phylogenetic information, we reanalysed their data set such that the assumption of independence was not violated. If Heffner and Masterton's hypothesis is correct, then one would expect evidence of strong correlated evolution between corticospinal tract anatomy and digital dexterity once the effects of the phylogenetic relationships between the species in the data set have been removed. The results show that a distinct bias in the number of primate species sampled by Heffner and Masterton significantly affected their findings. Furthermore, once phylogeny has been taken into account, only the length of the corticospinal tract fibres showed a significant relationship with two out of the four behaviours analysed, digital dexterity and hand-eye coordination. Based upon our results we recommend the use of modern comparative statistics for synthesising neural structure and behaviour, rather than examining structure function relationships in an ahistorical context. It is also evident that there is a need for data on the length and depth of the corticospinal fibres for a greater range of species so that the relationship between the corticospinal tract structure and motor behaviour for mammals as a whole can be more readily interpreted.