Arginine vasotocin (AVT) and its mammalian homologue, arginine vasopressin (AVP), regulate a variety of social and reproductive behaviors, often with complex species-, sex-, and context-dependent effects. Despite extensive evidence documenting seasonal variation in brain AVT/AVP, relatively few studies have investigated the environmental and/or hormonal factors mediating these seasonal changes. In the present study, we investigated whether the pineal hormone melatonin alters brain AVT immunoreactivity in green treefrogs (Hyla cinerea). Reproductively active male and female frogs were collected during the summer breeding season and a melatonin-filled or blank silastic capsule was surgically implanted subcutaneously. The duration of hormone treatment was 4 weeks, at which time frogs were euthanized and the brains and blood collected and processed for AVT immunohistochemistry and steroid hormone assay. We quantified AVT-immunoreactive (AVT-ir) cell bodies in the nucleus accumbens (NAcc), caudal striatum and amygdala (AMG), anterior preoptic area (POA), suprachiasmatic nucleus (SCN), and infundibular region of the ventral hypothalamus (VH). Sex differences in AVT-ir cell number were observed in all brain regions except the anterior POA and VH, with males having more AVT-ir cells than females in the NAcc, AMG, and SCN. Brain AVT was sensitive to melatonin signaling during the breeding season, and the effects of melatonin varied significantly with both region and sex. Treatment with melatonin decreased AVT immunoreactivity in both the NAcc and SCN in male H. cinerea. In contrast, brain AVT was relatively insensitive to melatonin signaling in females, indicating that the regulation of the AVT/AVP neuropeptide system by melatonin may be sexually dimorphic. Finally, melatonin did not significantly influence testosterone or estradiol concentrations of male or female frogs, respectively, suggesting that the effects of melatonin on AVT immunoreactivity are independent of changes in gonadal sex steroid hormones. Collectively, our results indicate that the AVT/AVP neuronal system may be an important target for melatonin in facilitating seasonal changes in reproductive physiology and social behavior.
Melatonin; Arginine vasotocin; Immunoreactivity; Testosterone; Estradiol; Sex differences; Amphibian
Vesicular glutamate transporters reuptake glutamate into synaptic vesicles at excitatory synapses. Vesicular glutamate transporter 2 (VGLUT2) is localized in the cortical terminals of neuronal somas located in the main sensory nuclei of the thalamus. Thus, immunolabeling of cortex with antibodies to VGLUT2 can reveal geniculostriate terminal distributions in species in which connectivity cannot be studied with tract-tracing techniques, permitting broader comparative studies of cortical specializations. Here, we used VGLUT2 immunohistochemistry to compare the organization of geniculostriate afferents in primary visual cortex in hominid primates (humans, chimpanzees, orangutan), Old World monkeys (rhesus macaques, vervets), and New World monkeys (squirrel monkeys). The New World and Old World monkeys had a broad, dense band of terminal-like labeling in cortical layer 4C, a narrow band of labeling in layer 4A, and additional labeling in layers 2/3 and 6, consistent with results from conventional tract-tracing studies in these species. By contrast, although the hominid primates had a prominent layer 4C band, labeling of layer 4A was sparse or absent. Label was also present in layers 2/3 and 6, although labeling of layer 6 in hominids was weaker and possibly more individually variable than in Old World and New World monkeys. These findings are consistent with previous observations from cytochrome oxidase histochemistry and a very small number of connectivity studies, suggesting that the projection from the parvocellular layers of the lateral geniculate nucleus to layer 4A were strongly reduced or eliminated in humans and apes following their evolutionary divergence from the other anthropoid primates.
Vesicular glutamate transporter; Area 17; Primary visual cortex; Architectonics; Primate; Human; Blobs; Evolution; Chimpanzees
Short-tailed opossums (Monodelphis domestica) belong to the branch of marsupial mammals that diverged from eutherian mammals approximately 180 million years ago. They are small in size, lack a marsupial pouch, and may have retained more morphological characteristics of early marsupial neocortex than most other marsupials. In the present study, we used several different histochemical and immunochemical procedures to reveal the architectonic characteristics of cortical areas in short-tailed opossums. Subdivisions of cortex were identified in brain sections cut in the coronal, sagittal, horizontal or tangential planes and processed for a calcium-binding protein, parvalbumin (PV), neurofilament protein epitopes recognized by SMI-32, the vesicle glutamate transporter 2 (VGluT2), myelin, cytochrome oxidase (CO), and Nissl substance. These different procedures revealed similar boundaries among areas, suggesting that functionally relevant borders were detected. The results allowed a fuller description and more precise demarcation of previously identified sensory areas, and the delineation of additional subdivisions of cortex. Area 17 (V1) was especially prominent, with a densely populated layer 4, high myelination levels, and dark staining of PV and VGluT2 immunopositive terminations. These architectonic features were present, albeit less pronounced, in somatosensory and auditory cortex. The major findings support the conclusion that short-tailed opossums have fewer cortical areas and their neocortex is less distinctly laminated than most other mammals.
Marsupial; Cortical areas; Visual cortex; Frontal cortex; Somatosensory cortex; Auditory cortex; Retrosplenial cortex; Cingulate cortex
The physiological state of animals in many taxonomic groups can be modified via social interactions, including simply receiving communication signals from conspecifics. Here, we explore whether the catecholaminergic system of female songbirds responds during social interactions that are limited to song reception. We measured the protein product of an immediate early gene (ZENK) within three catecholaminergic brain regions in song-exposed (N = 11) and silent-exposed (N = 6) female zebra finches (Taeniopygia guttata). ZENK-ir induction was quantified in catecholamine cells as well as within cells of unknown phenotypes in three brain regions that synthesize catecholamines, the ventral tegmental area (VTA), the periaqueductal gray (PAG) and the locus coeruleus (LoC). Our results reveal that there are no significant differences in the overall number of cells expressing ZENK between song-exposed and silent-exposed females. However, when we limited our measurements to catecholamine-containing cells, we show a greater number of catecholamine-containing cells expressing ZENK within the LoC in the song-exposed females as compared to silent-exposed females. Furthermore, we measured five behaviors during the song and silent-exposed period, as behavioral differences between these groups may account for differences in the co-induction of ZENK and TH-ir. Our results reveal that there were no statistically significant differences in the five measured behaviors between song and silent-exposed females. Our study demonstrates that noradrenergic cells within the LoC are involved in the neural architecture underlying sound perception and that cells within the catecholaminergic system are modulated by social interactions, particularly the reception of signals used in animal communication.
Noradrenaline; Catecholamine; Immediate Early Gene; Animal Communication; Songbird; dopamine; communication
Gonadal steroid hormones have been shown to influence adult neurogenesis in addition to their well-defined role in regulating social behavior. Adult neurogenesis consists of several processes including cell proliferation, which can be studied via 5-bromo-2′-deoxyuridine (BrdU) labeling. In a previous study we found that social stimulation altered both cell proliferation and levels of circulating gonadal steroids, leaving the issue of cause/effect unclear. In this study, we sought to determine whether socially modulated BrdU-labeling depends on gonadal hormone changes. We investigated this using a gonadectomy-implant paradigm and by exposing male and female green treefrogs (Hyla cinerea) to their conspecific chorus or control stimuli (i.e. random tones). Our results indicate that socially modulated cell proliferation occurred independently of gonadal hormone levels; furthermore, neither androgens in males nor estrogen in females increased cell proliferation in the preoptic area (POA) and infundibular hypothalamus, brain regions involved in endocrine regulation and acoustic communication. In fact, elevated estrogen levels decreased cell proliferation in those brain regions in the implanted female. In male frogs, evoked calling behavior was positively correlated with BrdU-labeling in the POA; however, statistical analysis showed that this behavior did not mediate socially induced cell proliferation. These results show that the social modulation of cell proliferation can occur without gonadal hormone involvement in either male or female adult anuran amphibians, and confirms that it is independent of a behavioral response in males.
Amphibian; Cell proliferation; BrdU; Neurogenesis; Acoustic communication; Social behavior; Estrogen; Testosterone
In environments where resources are difficult to obtain and enhanced cognitive capabilities might be adaptive, brain structures associated with cognitive traits may also be enhanced. In our previous studies, we documented a clear and significant relationship among environmental conditions, memory and hippocampal structure using ten populations of black-capped chickadees (Poecile atricapillus) over a large geographic range. In addition, focusing on just the two populations from the geographical extremes of our large-scale comparison, Alaska and Kansas, we found enhanced problem-solving capabilities and reduced neophobia in a captive-raised population of black-capped chickadees originating from the energetically demanding environment (Alaska) relative to conspecifics from the milder environment (Kansas). Here, we focused on three brain regions, the arcopallium (AP), the nucleus taeniae of the amygdala and the lateral striatum (LSt), that have been implicated to some extent in aspects of these behaviors in order to investigate whether potential differences in these brain areas may be associated with our previously detected differences in cognition. We compared the variation in neuron number and volumes of these regions between these populations, in both wild-caught birds and captive-raised individuals. Consistent with our behavioral observations, wild-caught birds from Kansas had a larger AP volume than their wild-caught conspecifics from Alaska, which possessed a higher density of neurons in the LSt. However, there were no other significant differences between populations in the wild-caught and captive-raised groups. Interestingly, individuals from the wild had larger LSt and AP volumes with more neurons than those raised in captivity. Overall, we provide some evidence that population-related differences in problem solving and neophobia may be associated with differences in volume and neuron numbers of our target brain regions. However, the relationship is not completely clear, and our study raises numerous questions about the relationship between the brain and behavior, especially in captive animals.
Amygdala; Arcopallium; Avian brain; Fear; Lateral striatum; Learning; Nucleus taeniae of the amygdala
Transmitting information via communicative signals is integral to interacting with conspecifics, and some species achieve this task by varying vocalizations to reflect context. Although signal variation is critical to social interactions, the underlying neural control has not been studied. In response to a predator, black-capped chickadees (Poecile atricapilla) produce mobbing calls (chick-a-dee calls) with various parameters, some of which convey information about the threat stimulus. We predicted that vocal parameters indicative of threat would be associated with distinct patterns of neuronal activity within brain areas involved in social behavior and those involved in the sensorimotor control of vocal production. To test this prediction, we measured the syntax and structural aspects of chick-a-dee call production in response to a hawk model and assessed the protein product of the immediate early gene FOS in brain regions implicated in context-specific vocal and social behavior. These regions include the medial preoptic area (POM) and lateral septum (LS), as well as regions involved in vocal motor control, including the dorsomedial nucleus of the intercollicular complex and the HVC. We found correlations linking call rate (previously demonstrated to reflect threat) to labeling in the POM and LS. Labeling in the HVC correlated with the number of D notes per call, which may also signal threat level. Labeling in the call control region dorsomedial nucleus was associated with the structure of D notes and the overall number of notes, but not call rate or type of notes produced. These results suggest that the POM and LS may influence attributes of vocalizations produced in response to predators and that the brain region implicated in song control, the HVC, also influences call production. Because variation in chick-a-dee call rate indicates predator threat, we speculate that these areas could integrate with motor control regions to imbue mobbing signals with additional information about threat level.
Lateral septum; Medial preoptic area; Alarm call; Anti-predator display; Black-capped chickadee
Evidence has accumulated that the regulation of male sexual behavior by dopamine may not be the same in Japanese quail (and perhaps all birds) as it is in mammals. For example, the non-selective dopamine receptor agonist, apomorphine (APO) facilitates male sexual behavior in rats but inhibits it in quail. Although the general organization of the dopamine system is similar in birds and mammals, it is possible that the relative distribution and/or density of binding sites is different. We therefore compared the relative densities of D1-like and D2-like receptor subtypes in Japanese quail and rats, with the use of in vitro quantitative receptor autoradiography. Brain sections from 8 male rats and 8 male quail were labeled with [3H]SCH-23390 and [3H]Spiperone. In general we found a systematic species difference in the relative density of D1-like vs. D2-like receptors such that the D2/D1 ratio is higher in quail than in rats in areas well known to be important target sites for dopamine action such as striatal regions. We also uncovered significant differences in the relative density of D1-like and D2-like receptors in brain areas associated with sexual behavior, including the preoptic area, such that there was a greater D2/D1 ratio in quail as compared to rats. This difference may explain the variation in the behavioral effectiveness of APO in rats as compared to quail; with a higher relative density of D2-like receptors in quail, a similar dose of APO would be more likely to activate inhibitory processes in quail than in rats.
dopamine; autoradiography; apomorphine; male sexual behavior; bird
This paper reviews some of the major evidence and arguments currently available to support the view that human speech perception may require the use of specialized neural mechanisms for perceptual analysis. Experiments using synthetically produced speech signals with adults are briefly summarized and extensions of these results to infants and other organisms are reviewed with an emphasis towards detailing those aspects of speech perception that may require some need for specialized species-specific processors. Finally, some comments on the role of early experience in perceptual development are provided as an attempt to identify promising areas of new research in speech perception.
Speech perception; Synthetic speech; Identification; Discrimination; Species-specific acoustic signals; Perceptual development; Feature detectors; Perceptual constancy; Speech mode
Predation pressure represents a strong selective force that influences the development and evolution of living organisms. An increasing number of studies have shown that both environmental and social factors, including exposure to predators, substantially shape the structure and function of the brain. However, our knowledge about the molecular mechanisms underlying the response of the brain to environmental stimuli is limited. In this study, we used whole-genome comparative oligonucleotide microarrays to investigate the brain transcriptomic response to cues of a predator in the threespine stickleback, Gasterosteus aculeatus. We found that repeated exposure to olfactory, visual and tactile cues of a predator (rainbow trout, Oncorrhynchus mykiss) for 6 days resulted in subtle but significant transcriptomic changes in the brain of sticklebacks. Gene functional analysis and gene ontology enrichment revealed that the majority of the transcripts differentially expressed between the fish exposed to cues of a predator and the control group were related to antigen processing and presentation involving the major histocompatibility complex, transmission of synaptic signals, brain metabolic processes, gene regulation and visual perception. The top four identified pathways were synaptic long-term depression, RAN signaling, relaxin signaling and phototransduction. Our study demonstrates that exposure of sticklebacks to cues of a predator results in the activation of a wide range of biological and molecular processes and lays the foundation for future investigations on the molecular factors that modulate the function and evolution of the brain in response to stressors.
Neurogenomics; Stress; Predation; Microarray; Gene expression; Gasterosteus aculeatus
We previously reported that in a eusocial rodent, the naked mole-rat (Heterocephalus glaber), traditional neural sex differences were absent; instead, neural dimorphisms were associated with breeding status. Here we examined the same neural regions previously studied in naked mole-rats in a second eusocial species, the Damaraland mole-rat (Fukomys damarensis). Damaraland mole-rats live in social groups with breeding restricted to a small number of animals. However, colony sizes are much smaller in Damaraland mole-rats than in naked mole-rats and there is consequently less reproductive skew. In this sense, Damaraland mole-rats may be considered intermediate in social organization between naked mole-rats and more traditional laboratory rodents. We report that, as in naked mole-rats, breeding Damaraland mole-rats have larger volumes of the principal nucleus of the bed nucleus of the stria terminalis and paraventricular nucleus of the hypothalamus than do subordinates, with no effect of sex on these measures. Thus, these structures may play special roles in breeders of eusocial species. However, in contrast to what was seen in naked mole-rats, we also found sex differences in Damaraland mole-rats: volume of the medial amygdala and motoneuron number in Onuf's nucleus were both greater in males than in females, with no significant effect of breeding status. Thus, both sex and breeding status influence neural morphology in Damaraland mole-rats. These findings are in accord with the observed sex differences in body weight and genitalia in Damaraland but not naked mole-rats. We hypothesize that the increased sexual dimorphism in Damaraland mole-rats relative to naked mole-rats is related to reduced reproductive skew.
Bed nucleus of the stria terminalis; Damaraland mole-rat; Medial amygdala; Naked mole-rat; Onuf's nucleus; Paraventricular nucleus; Sex difference; Social status
Rodents are a major order of mammals that is highly diverse in distribution and lifestyle. Five suborders, 34 families, and 2,277 species within this order occupy a number of different niches and vary along several lifestyle dimensions such as diel pattern (diurnal vs. nocturnal), terrain niche, and diet. For example, the terrain niche of rodents includes arboreal, aerial, terrestrial, semi-aquatic, burrowing, and rock dwelling. Not surprisingly, the behaviors associated with particular lifestyles are also highly variable and thus the neocortex, which generates these behaviors, has undergone corresponding alterations across species. Studies of cortical organization in species that vary along several dimensions such as terrain niche, diel pattern, and rearing conditions demonstrate that the size and number of cortical fields can be highly variable within this order. The internal organization of a cortical field also reflects lifestyle differences between species and exaggerates behaviorally relevant effectors such as vibrissae, teeth, or lips. Finally, at a cellular level, neuronal number and density varies for the same cortical field in different species and is even different for the same species reared in different conditions (laboratory vs. wild-caught). These very large differences across and within rodent species indicate that there is no generic rodent model. Rather, there are rodent models suited for specific questions regarding the development, function, and evolution of the neocortex.
Rats; Mice; Somatosensory cortex; Visual cortex; Auditory cortex; Motor cortex; Evolution
In the bullfrog (Rana catesbeiana), the process of metamorphosis culminates in the appearance of new visual and visuomotor behaviors reflective of the emergence of binocular vision and visually-guided prey capture behaviors as the animal transitions to life on land. Using several different neuroanatomical tracers, we examined the substrates that may underlie these behavioral changes by tracing the afferent and efferent connectivity of the midbrain optic tectum across metamorphic development. Intratectal, tectotoral, tectotegmental, tectobulbar, and tecto-thalamic tracts exhibit similar trajectories of neurobiotin fiber label across the developmental span from early larval tadpoles to adults. Developmental variability was apparent primarily in intensity and distribution of cell and puncta label in target nuclei. Combined injections of cholera toxin subunit β and Phaseolus vulgaris leucoagglutinin consistently label cell bodies, puncta, or fiber segments bilaterally in midbrain targets including the pretectal gray, laminar nucleus of the torus semicircularis, and the nucleus of the medial longitudinal fasciculus. Developmentally stable label was observed bilaterally in medullary targets including the medial vestibular nucleus, lateral vestibular nucleus, and reticular gray, and in forebrain targets including the posterior and ventromedial nuclei of the thalamus. The nucleus isthmi, cerebellum, lateral line nuclei, medial septum, ventral striatum, and medial pallium show more developmentally variable patterns of connectivity. Our results suggest that even during larval development, the optic tectum contains substrates for integration of visual with auditory, vestibular, and somatosensory cues, as well as for guidance of motivated behaviors.
Medial septum; Metamorphosis; Midbrain; Multisensory convergence; Nucleus isthmi; Optic tectum; Tadpole; Thalamus
Brain size scales as different functions of its number of neurons across mammalian orders such as rodents, primates, and insectivores. In rodents, we have previously shown that, across a sample of 6 species, from mouse to capybara, the cerebral cortex, cerebellum and the remaining brain structures increase in size faster than they gain neurons, with an accompanying decrease in neuronal density in these structures [Herculano-Houzel et al.: Proc Natl Acad Sci USA 2006;103:12138–12143]. Important remaining questions are whether such neuronal scaling rules within an order apply equally to all pertaining species, and whether they extend to closely related taxa. Here, we examine whether 4 other species of Rodentia, as well as the closely related rabbit (Lagomorpha), conform to the scaling rules identified previously for rodents. We report the updated neuronal scaling rules obtained for the average values of each species in a way that is directly comparable to the scaling rules that apply to primates [Gabi et al.: Brain Behav Evol 2010;76:32–44], and examine whether the scaling relationships are affected when phylogenetic relatedness in the dataset is accounted for. We have found that the brains of the spiny rat, squirrel, prairie dog and rabbit conform to the neuronal scaling rules that apply to the previous sample of rodents. The conformity to the previous rules of the new set of species, which includes the rabbit, suggests that the cellular scaling rules we have identified apply to rodents in general, and probably to Glires as a whole (rodents/lagomorphs), with one notable exception: the naked mole-rat brain is apparently an outlier, with only about half of the neurons expected from its brain size in its cerebral cortex and cerebellum.
Rodents; Brain size; Evolution; Neurons; Glia; Glires
Differences in cognitive abilities and the relatively large brain are among the most striking differences between humans and their closest primate relatives. The energy trade-off hypothesis predicts that a major shift in energy allocation among tissues occurred during human origins in order to support the remarkable expansion of a metabolically expensive brain. However, the molecular basis of this adaptive scenario is unknown. Two glucose transporters (SLC2A1 and SLC2A4) are promising candidates and present intriguing mutations in humans, resulting, respectively, in microcephaly and disruptions in whole-body glucose homeostasis. We compared SLC2A1 and SLC2A4 expression between humans, chimpanzees and macaques, and found compensatory and biologically significant expression changes on the human lineage within cerebral cortex and skeletal muscle, consistent with mediating an energy trade-off. We also show that these two genes are likely to have undergone adaptation and participated in the development and maintenance of a larger brain in the human lineage by modulating brain and skeletal muscle energy allocation. We found that these two genes show human-specific signatures of positive selection on known regulatory elements within their 5′-untranslated region, suggesting an adaptation of their regulation during human origins. This study represents the first case where adaptive, functional and genetic lines of evidence implicate specific genes in the evolution of human brain size.
Glucose; Transporters; Brain; Evolution; Primates
Biologists have long been interested in both the regularities and the deviations in the relationship between brain, development, ecology, and behavior between taxa. We first examine some basic information about the observed ranges of fundamental changes in developmental parameters (i.e. neurogenesis timing, cell cycle rates, and gene expression patterns) between taxa. Next, we review what is known about the relative importance of different kinds of developmental mechanisms in producing brain change, focusing on mechanisms of segmentation, local and general features of neurogenesis, and cell cycle kinetics. We suggest that a limited set of developmental alterations of the vertebrate nervous system typically occur and that each kind of developmental change may entail unique anatomical, functional, and behavioral consequences for the organism. Thus, neuroecologists who posit a direct mapping of brain size to behavior should consider that not any change in brain anatomy is possible.
Neurogenesis; Evolution; Development; Mammals; Birds
In this study we examine the size of primary sensory areas in the neocortex and the cellular composition of area 17/V1 in three rodent groups: laboratory nocturnal Norway rats (Long-Evans; Rattus norvegicus), wild-caught nocturnal Norway rats (R. norvegicus), and laboratory diurnal Nile grass rats (Arvicanthis niloticus). Specifically, we used areal measures of myeloarchitecture of the primary sensory areas to compare area size and the isotropic fractionator method to estimate the number of neurons and nonneurons in area 17 in each species. Our results demonstrate that the percentage of cortex devoted to area 17 is significantly greater and the percentage of cortex devoted to S1 is significantly smaller in the diurnal Nile grass rat compared with the nocturnal Norway rat groups. Further, the laboratory rodent groups have a greater percentage of cortex devoted to auditory cortex compared with the wild-caught group. We also demonstrate that wild-caught rats have a greater density of neurons in area 17 compared to laboratory-reared animals. However, there were no other clear cellular composition differences in area 17 or differences in the percentage of brain weight devoted to area 17 between nocturnal and diurnal rats. Thus, there are differences in primary sensory area size between diurnal versus nocturnal and laboratory versus wild-caught rat groups and cellular density between wild-caught and laboratory rat groups. Our results demonstrate that the differences in the size and cellular composition of cortical areas do not fit with what would be expected based on brain scaling differences alone, and have a consistent relationship with lifestyle and sensory morphology.
Architecture; Area 17; Cellular composition; Evolution; Isotropic fractionator; Vision
Gorillas and orangutans are primates at least as large as humans, but their brains amount to about one third of the size of the human brain. This discrepancy has been used as evidence that the human brain is about 3 times larger than it should be for a primate species of its body size. In contrast to the view that the human brain is special in its size, we have suggested that it is the great apes that might have evolved bodies that are unusually large, on the basis of our recent finding that the cellular composition of the human brain matches that expected for a primate brain of its size, making the human brain a linearly scaled-up primate brain in its number of cells. To investigate whether the brain of great apes also conforms to the primate cellular scaling rules identified previously, we determine the numbers of neuronal and other cells that compose the orangutan and gorilla cerebella, use these numbers to calculate the size of the brain and of the cerebral cortex expected for these species, and show that these match the sizes described in the literature. Our results suggest that the brains of great apes also scale linearly in their numbers of neurons like other primate brains, including humans. The conformity of great apes and humans to the linear cellular scaling rules that apply to other primates that diverged earlier in primate evolution indicates that prehistoric Homo species as well as other hominins must have had brains that conformed to the same scaling rules, irrespective of their body size. We then used those scaling rules and published estimated brain volumes for various hominin species to predict the numbers of neurons that composed their brains. We predict that Homo heidelbergensis and Homo neanderthalensis had brains with approximately 80 billion neurons, within the range of variation found in modern Homo sapiens. We propose that while the cellular scaling rules that apply to the primate brain have remained stable in hominin evolution (since they apply to simians, great apes and modern humans alike), the Colobinae and Pongidae lineages favored marked increases in body size rather than brain size from the common ancestor with the Homo lineage, while the Homo lineage seems to have favored a large brain instead of a large body, possibly due to the metabolic limitations to having both.
Allometry; Brain size; Great apes; Human; Evolution, human; Neurons, number
Increases in the size of the neuronal structures that mediate specific behaviors are believed to be related to enhanced computational performance. It is not clear, however, what developmental and evolutionary mechanisms mediate these changes, nor whether an increase in the size of a given neuronal population is a general mechanism to achieve enhanced computational ability. We addressed the issue of size by analyzing the variation in the relative number of cells of auditory structures in auditory specialists and generalists. We show that bird species with different auditory specializations exhibit variation in the relative size of their hindbrain auditory nuclei. In the barn owl, an auditory specialist, the hind-brain auditory nuclei involved in the computation of sound location show hyperplasia. This hyperplasia was also found in songbirds, but not in non-auditory specialists. The hyperplasia of auditory nuclei was also not seen in birds with large body weight suggesting that the total number of cells is selected for in auditory specialists. In barn owls, differences observed in the relative size of the auditory nuclei might be attributed to modifications in neurogenesis and cell death. Thus, hyperplasia of circuits used for auditory computation accompanies auditory specialization in different orders of birds.
Evolution; Auditory; Neuronal computation; Birds; Allometry
On the basis of patterns of anterograde, retrograde, and bi-directional transport of tracers from both the superior olivary nucleus (SON) and the torus semicircularis (TS), we report anatomical changes in brainstem connectivity across metamorphic development in the bullfrog, Rana catesbeiana. In early and late stages of larval development (Gosner stages 25–37), anterograde or bi-directional tracers injected into the SON produce terminal/fiber label in the contralateral SON and in the ipsilateral TS. Between stages 38–41 (deaf period), only sparse or no terminal/fiber label is visible in these target nuclei. During metamorphic climax (stages 42–46), terminal/fiber label reappears in both the contralateral SON and in the ipsilateral TS, and now also in the contralateral TS. Injections of retrograde tracers into the SON fail to label cell bodies in the ipsilateral TS in deaf period animals, mirroring the previously-reported failure of retrograde transport from the TS to the ipsilateral SON during this developmental time. Bilateral cell body label emerges in the dorsal medullary nucleus and the lateral vestibular nucleus bilaterally as a result of SON transport during the late larval period, while cell body label in the contralateral TS emerges during climax. At all larval stages, injections into the SON produce anterograde and retrograde label in the medial vestibular nucleus bilaterally. These data show anatomical stability in some pathways and plasticity in others during larval development, with the most dramatic changes occurring during the deaf period and metamorphic climax. Animals in metamorphic climax show patterns of connectivity similar to that of froglets and adults, indicating the maturation during climax of central anatomical substrates for hearing in air.
Tadpoles; Anurans; Vestibular nucleus complex; Dorsal medullary nucleus; Superior olivary complex; Torus semicircularis; Lipophilic dyes; PHA-L; Cholera toxin; Metamorphosis
Growth-associated protein-43 is typically expressed at high levels in the nervous system during development. In adult animals, its expression is lower, but still observable in brain areas showing structural or functional plasticity. We examined patterns of GAP-43 immunoreactivity in the brain of the bullfrog, an animal whose nervous system undergoes considerable reorganization across metamorphic development and retains a strong capacity for plasticity in adulthood. Immunolabeling was mostly diffuse in hatchling tadpoles, but became progressively more discrete as larval development proceeded. In many brain areas, intensity of immunolabel peaked at metamorphic climax, the time of final transition from aquatic to semi-terrestrial life. Changes in intensity of GAP-43 expression in the medial vestibular nucleus, superior olivary nucleus, and torus semicircularis appeared correlated with stage-dependent functional changes in processing auditory stimuli. Immunolabeling in the Purkinje cell layer of the cerebellum and in the cerebellar nucleus was detectable at most developmental time points. Heavy immunolabel was present from early larval stages through the end of climax in the thalamus (ventromedial, anterior, posterior, central nuclei). Immunolabel in the tadpole telencephalon was observed around the lateral ventricles, and in the medial septum and ventral striatum. In postmetamorphic animals, immunoreactivity was confined mainly to the ventricular zones and immediately adjacent cell layers. GAP-43 expression was present in olfactory, auditory and optic cranial nerves throughout larval and postmetamorphic life. The continued expression of GAP-43 in brain nuclei and in cranial nerves throughout development and into adulthood reflects the high regenerative potential of the bullfrog’s central nervous system.
Growth-associated protein 43; Plasticity; Metamorphosis; Bullfrog; Midbrain; Forebrain; Cranial nerves
The distribution of proliferating cells in the midbrain, thalamus, and telencephalon of adult bullfrogs (Rana catesbeiana) was examined using immunohistochemistry for the thymidine analog 5-bromo-2′-deoxyuridine (BrdU) and DNA dot-blotting. At all time points examined (2 to 28 days post-injection), BrdU-labeled cells were located in ventricular zones at all levels of the neuraxis, but with relatively more label around the telencephalic ventricles. Labeled cells, some showing profiles indicative of dividing and migrating cells, were present in brain parenchyma from 7 to 28 days post-injection. These labeled cells were particularly numerous in the dorsal and ventral hypothalamus, preoptic area, optic tectum, and laminar and principal nuclei of the torus semicircularis, with label also present, but at qualitatively reduced levels, in thalamic and telencephalic nuclei. Double-label immunohistochemistry using glial and early neural markers indicated that gliogenesis and neurogenesis both occurred, with new neurons observed particularly in the hypothalamus, optic tectum, and torus semicircularis. In all brain areas, many cells not labeled with BrdU were nonetheless labeled with the early neural marker TOAD-64, indicating that these cells were postmitotic. Incorporation of DNA measured by dot-blotting confirms the presence of DNA synthesis in the forebrain and brainstem at all time points measured. The pattern of BrdU label confirms previous experiments based on labeling with 3H-thymidine and proliferating cell nuclear antigen showing cell proliferation in the adult ranid brain, particularly in hypothalamic nuclei. The consistent appearance of new cells in the hypothalamus of adult frogs suggests that proliferative activity may be important in mediating reproductive behaviors in these animals.
Cell proliferation; Neurogenesis; Gliogenesis; Amphibians; Bullfrog
Voxel-based morphometry (VBM) has become an increasingly common method for assessing neuroanatomical asymmetries in human in vivo magnetic resonance imaging (MRI). Here, we employed VBM to examine asymmetries in white matter in a sample of 48 chimpanzees (15 males and 33 females). T1-weighted MRI scans were segmented into white matter using FSL and registered to a common template. The segmented volumes were then flipped in the left-right axis and registered back to the template. The mirror image white matter volumes were then subtracted from the correctly oriented volumes and voxel-by-voxel t tests were performed. Twenty-seven significant lateralized clusters were found, including 18 in the left hemisphere and 9 in the right hemisphere. Several of the asymmetries were found in regions corresponding to well-known white matter tracts including the superior longitudinal fasciculus, inferior longitudinal fasciculus and corticospinal tract.
Chimpanzees; Brain asymmetry; White matter; Language evolution
What are the rules relating the size of the brain and its structures to the number of cells that compose them and their average sizes? We have shown previously that the cerebral cortex, cerebellum and the remaining brain structures increase in size as a linear function of their numbers of neurons and non-neuronal cells across 6 species of primates. Here we describe that the cellular composition of the same brain structures of 5 other primate species, as well as humans, conform to the scaling rules identified previously, and that the updated power functions for the extended sample are similar to those determined earlier. Accounting for phylogenetic relatedness in the combined dataset does not affect the scaling slopes that apply to the cerebral cortex and cerebellum, but alters the slope for the remaining brain structures to a value that is similar to that observed in rodents, which raises the possibility that the neuronal scaling rules for these structures are shared among rodents and primates. The conformity of the new set of primate species to the previous rules strongly suggests that the cellular scaling rules we have identified apply to primates in general, including humans, and not only to particular subgroups of primate species. In contrast, the allometric rules relating body and brain size are highly sensitive to the particular species sampled, suggesting that brain size is neither determined by body size nor together with it, but is rather only loosely correlated with body size.
Allometry; Brain size; Evolution; Glia, number; Neurons, number; Primates
The spinal cord can be considered a major sensorimotor interface between the body and the brain. How does the spinal cord scale with body and brain mass, and how are its numbers of neurons related to the number of neurons in the brain across species of different body and brain sizes? Here we determine the cellular composition of the spinal cord in eight primate species and find that its number of neurons varies as a linear function of cord length, and accompanies body mass raised to an exponent close to 1/3. This relationship suggests that the extension, mass and number of neurons that compose the spinal cord are related to body length, rather than to body mass or surface. Moreover, we show that although brain mass increases linearly with cord mass, the number of neurons in the brain increases with the number of neurons in the spinal cord raised to the power of 1.7. This faster addition of neurons to the brain than to the spinal cord is consistent with current views on how larger brains add complexity to the processing of environmental and somatic information.
Allometry; Number of neurons; Evolution; Connectivity