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1.  Updated Neuronal Scaling Rules for the Brains of Glires (Rodents/Lagomorphs) 
Brain, Behavior and Evolution  2011;78(4):302-314.
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.
PMCID: PMC3237106  PMID: 21985803
Rodents; Brain size; Evolution; Neurons; Glia; Glires
2.  Plasticity of the worker bumble bee brain in relation to age and rearing environment 
Brain, behavior and evolution  2013;82(4):250-261.
The environment experienced during development can dramatically affect the brain, with possible implications for sensory processing, learning and memory. Although the effects of single sensory modalities on brain development have been repeatedly explored, the additive or interactive effects of multiple modalities have been less thoroughly investigated. We asked how experience with multisensory stimuli affected brain development in the bumble bee, Bombus impatiens. First, to establish the timeline of brain development during early adulthood, we estimated regional brain volumes across a range of ages. We discovered significant age-related volume changes in nearly every region of the brain. Next, to determine whether these changes were dependent upon certain environmental stimuli, we manipulated the visual and olfactory stimuli available to newly emerged bumble bee workers in a factorial manner. Newly emerged bumble bees were maintained in the presence or absence of supplemental visual and/or olfactory stimuli for seven days, after which the volumes of several brain regions were estimated. We found that the volumes of the mushroom body lobes and calyces were larger in the absence of visual stimuli. Additionally, visual deprivation was associated with the expression of larger antennal lobes, the primary olfactory processing regions of the brain. In contrast, exposure to plant-derived olfactory stimuli did not have a significant effect on brain region volumes. This study is the first to explore the separate and interactive effects of visual and olfactory stimuli on bee brain development. Assessing the timing and sensitivity of brain development is a first step toward understanding how different rearing environments differentially affect regional brain volumes in this species. Our findings suggest that environmental factors experienced during the first week of adulthood can modify bumble brain development in many subtle ways.
PMCID: PMC3905614  PMID: 24281415
neuronal plasticity; Bombus; sensory environment; mushroom bodies; multimodal interactions
3.  Things Change – How Comparative Transcriptomics Suggests the Pallium has Evolved at Multiple Levels of Organization 
Brain, behavior and evolution  2013;82(3):10.1159/000354969.
PMCID: PMC3881543  PMID: 24081114
Wulst; transcriptomics; sequencing; pallium; homology; cerebral cortex; brain evolution; Cell-type homology/equivalent circuit hypothesis; deep homology; dorsal ventricular ridge
4.  Sexual dimorphism in the brain of the monogamous California mouse (Peromyscus californicus) 
Brain, behavior and evolution  2013;81(4):236-249.
Sex differences in behavior and morphology are usually assumed to be stronger in polygynous species compared to monogamous species. A few brain structures have been identified as sexually dimorphic in polygynous rodent species, but it is less clear whether these differences persist in monogamous species. California mice are among the 5% of mammals that are considered to be monogamous and as such provide an ideal model to examine sexual dimorphism in neuroanatomy. In the present study we compared the volume of hypothalamic and limbic associated regions in female and male California mice for sexual dimorphism. We also used tyrosine hydroxylase immunohistochemistry to compare the number of dopamine neurons in the ventral tegmental area (VTA) in female and male California mice. Additionally, tract tracing was used to accurately delineate the boundaries of the VTA. The total volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA), the principal nucleus of the bed nucleus of the stria terminalis, and the posterodorsal medial amygdala (MEApd) was larger in males compared to females. In the SDN-POA we found that the magnitude of sex differences in the California mouse were intermediate between the large differences observed in promiscuous meadow voles and rats and the absence of significant differences in monogamous prairie voles. However, the magnitude of sex differences in medial amygdala and the bed nucleus of the stria terminalis were comparable to polygynous species. No sex differences were observed in the volume of the whole brain, the VTA, the nucleus accumbens or the number of TH-ir neurons in the VTA. These data show that despite a monogamous social organization, sexual dimorphisms that have been reported in polygynous rodents extend to California mice. Our data suggest that sex differences in brain structures such as the SDN-POA persist across species with different social organizations and may be an evolutionarily conserved characteristic of mammalian brains.
PMCID: PMC3915401  PMID: 23881046
5.  Rhesus macaques recognize unique multi-modal face-voice relations of familiar individuals and not of unfamiliar ones 
Brain, behavior and evolution  2013;81(4):219-225.
Communication signals in non-human primates are inherently multi-modal. However, for laboratory-housed monkeys, there is relatively little evidence in support of the use of multi-modal communication signals in individual recognition. Here, we used a preferential-looking paradigm to test whether laboratory-housed rhesus could “spontaneously” (i.e., in the absence of operant training) use multi-modal communication stimuli to discriminate between known conspecifics. The multi-modal stimulus was a silent movie of two monkeys vocalizing and an audio file of the vocalization from one of the monkeys in the movie. We found that the gaze patterns of those monkeys that knew the individuals in the movie were reliably biased toward the individual that did not produce the vocalization. In contrast, there was not a systematic gaze pattern for those monkeys that did not know the individuals in the movie. These data are consistent with the hypothesis that laboratory-housed rhesus can recognize and distinguish between conspecifics based on auditory and visual communication signals.
PMCID: PMC3991244  PMID: 23774779
rhesus; communication; vocalization; multi-modal; auditory; facial cue
6.  Pheromone exposure influences preoptic arginine vasotocin gene expression and inhibits social approach behavior in response to rivals, but not potential mates 
Brain, behavior and evolution  2013;81(3):194-202.
The nonapeptides arginine vasotocin (AVT) and vasopressin (AVP) mediate a variety of social behaviors in vertebrates. However, the effects of these peptides on behavior can vary considerably both between and within species. AVT, in particular, stimulates aggressive and courtship responses typical of dominant males in several species, although it can also inhibit social interactions in some cases. Such differential effects may depend upon AVT influences within brain circuits that differ among species or between males that adopt alternative reproductive phenotypes and/or upon the differential activation of those circuits in different social contexts. However, to date, very little is known about how social stimuli that promote alternative behavioral responses influence AVT circuits within the brain. To address this issue, we exposed adult male goldfish to androstenedione (AD), a pheromonal signal that is released by both males and females during the breeding season, and measured social approach responses of males towards same- and other-sex individuals before and after AD exposure. In a second experiment, we measured AD-induced AVT gene expression using in situ hybridization. We found that brief exposure to AD induces social avoidance in response to rival males, but does not affect the level of sociality exhibited in response to sexually receptive females. Exposure to AD also increases AVT gene expression in the preoptic area of male goldfish, particularly in the parvocellular population of the preoptic nucleus. Together, these data suggest that AD is part of a social signaling system that induces social withdrawal specifically during male-male interactions by activating AVT neurons.
PMCID: PMC3755448  PMID: 23712040
arginine vasotocin; parvocellular preoptic area; social behavior; teleost; androstenedione
7.  NSF Workshop Report: Discovering General Principles of Nervous System Organization by Comparing Brain Maps across Species 
Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system ‘maps’ comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of ‘reference species’ to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution.
PMCID: PMC4028317  PMID: 24603302
8.  How Brains Are Built: Genetics and Evolution 
Brain, behavior and evolution  2013;81(2):71-73.
PMCID: PMC3632431  PMID: 23466525
9.  Lamination of the Lateral Geniculate Nucleus of Catarrhine Primates 
Brain, behavior and evolution  2013;81(2):93-108.
The lateral geniculate nucleus (LGN) of catarrhines – with the exception of gibbons – is typically described as a six-layered structure, comprised of two ventral magnocellular layers, and four dorsal parvocellular layers. The parvocellular layers of the LGN are involved in color vision. Therefore, it is hypothesized that a six-layered LGN is a shared-derived trait among catarrhines. This might suggest that in gibbons the lack of further subdivisions of the parvocellular layers is a recent change, and could be related to specializations of visual information processing in this taxon. To address these hypotheses, the lamination of the LGN was investigated in a range of catarrhine species, including several taxa not previously described, and the evolution of the LGN was reconstructed using phylogenetic information. The findings indicate that while all catarrhine species have four parvocellular leaflets, two main patterns of LGN parvocellular lamination occur: two undivided parvocellular layers in some species, and four parvocellular leaflets (with occasional subleaflets) in other species. LGN size was not found to be related to lamination pattern. Both patterns were found to occur in divergent clades, which is suggestive of homoplasy within the catarrhines in LGN morphology.
PMCID: PMC3741618  PMID: 23467282
evolution; phylogeny; catarrhines; primates; vision; lateral geniculate nucleus; parvocellular
10.  Variation in human brains may facilitate evolutionary change toward a limited range of phenotypes 
Brain, behavior and evolution  2013;81(2):74-85.
Individual variation is the foundation for evolutionary change, but little is known about the nature of normal variation between brains. Phylogenetic variation across mammalian brains is characterized by high inter-correlations in brain region volumes, distinct allometric scaling for each brain region and the relative independence in olfactory and limbic structures volumes from the rest of the brain. Previous work examining brain variation in individuals of some domesticated species showed that these three features of phylogenetic variation were mirrored in individual variation. We extend this analysis to the human brain and 10 of its subdivisions (e.g., isocortex, hippocampus) by using magnetic resonance imaging scans of 90 human brains ranging between 16 to 25 years of age. Human brain variation resembles both the individual variation seen in other species, and variation observed across mammalian species. That is, the relative differences in the slopes of each brain region compared to medulla size within humans and between mammals are concordant, and limbic structures scale with relative independence from other brain regions. This non-random pattern of variation suggests that developmental programs channel the variation available for selection.
PMCID: PMC3658611  PMID: 23363667
Allometry; Variation; Human; Brain; Evolution
11.  Spinal transection induces widespread proliferation of cells along the length of the spinal cord in a weakly electric fish 
Brain, behavior and evolution  2012;80(4):269-280.
The ability to regenerate spinal cord tissue after tail amputation has been well studied in several species of teleost fish. The present study examined proliferation and survival of cells following complete spinal cord transection rather than tail amputation in the weakly electric fish Apteronotus leptorhynchus. To quantify cell proliferation along the length of the spinal cord, fish were given a single bromodeoxyuridine (BrdU) injection immediately after spinal transection or sham surgery. Spinal transection significantly increased the density of BrdU+ cells along the entire length of the spinal cord at 1 day post transection (dpt), and most newly generated cells survived up to 14 dpt. To examine longer term survival of the newly proliferated cells, BrdU was injected for 5 days after the surgery, and fish were sacrificed 14 or 30 dpt. Spinal transection significantly increased proliferation and/or survival, as indicated by an elevated density of BrdU+ cells in the spinal cords of spinally transected compared to sham-operated and intact fish. At 14 dpt, BrdU+ cells were abundant at all levels of the spinal cord. By 30 dpt, the density of BrdU+ cells decreased at all levels of the spinal cord except at the tip of the tail. Thus, newly generated cells in the caudal-most segment of the spinal cord survived longer than those in more rostral segments. Our findings indicate that spinal cord transection stimulates widespread cellular proliferation; however, there were regional differences in the survival of the newly generated cells.
PMCID: PMC3706082  PMID: 23147638
12.  Sexually Dimorphic Effects of Melatonin on Brain Arginine Vasotocin Immunoreactivity in Green Treefrogs (Hyla cinerea) 
Brain, behavior and evolution  2012;80(3):222-232.
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.
PMCID: PMC3506391  PMID: 22906877
Melatonin; Arginine vasotocin; Immunoreactivity; Testosterone; Estradiol; Sex differences; Amphibian
13.  Evidence for Ape and Human Specializations in Geniculostriate Projections from VGLUT2 Immunohistochemistry 
Brain, behavior and evolution  2012;80(3):210-221.
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.
PMCID: PMC3503454  PMID: 22889767
Vesicular glutamate transporter; Area 17; Primary visual cortex; Architectonics; Primate; Human; Blobs; Evolution; Chimpanzees
14.  An Architectonic Study of the Neocortex of the Short-Tailed Opossum (Monodelphis domestica) 
Brain, behavior and evolution  2009;73(3):206-228.
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.
PMCID: PMC3710711  PMID: 19546531
Marsupial; Cortical areas; Visual cortex; Frontal cortex; Somatosensory cortex; Auditory cortex; Retrosplenial cortex; Cingulate cortex
15.  Co-Localization of Immediate Early Genes in Catecholamine Cells after Song Exposure in Female Zebra Finches (Taeniopygia guttata) 
Brain, behavior and evolution  2012;79(4):252-260.
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.
PMCID: PMC3606879  PMID: 22572406
Noradrenaline; Catecholamine; Immediate Early Gene; Animal Communication; Songbird; dopamine; communication
16.  Socially Modulated Cell Proliferation Is Independent of Gonadal Steroid Hormones in the Brain of the Adult Green Treefrog (Hyla cinerea) 
Brain, Behavior and Evolution  2012;79(3):170-180.
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.
PMCID: PMC3343747  PMID: 22269468
Amphibian; Cell proliferation; BrdU; Neurogenesis; Acoustic communication; Social behavior; Estrogen; Testosterone
17.  Variation in Brain Regions Associated with Fear and Learning in Contrasting Climates 
Brain, Behavior and Evolution  2012;79(3):181-190.
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.
PMCID: PMC3343761  PMID: 22286546
Amygdala; Arcopallium; Avian brain; Fear; Lateral striatum; Learning; Nucleus taeniae of the amygdala
18.  Vocal Parameters That Indicate Threat Level Correlate with FOS Immunolabeling in Social and Vocal Control Brain Regions 
Brain, Behavior and Evolution  2011;79(2):128-140.
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.
PMCID: PMC3355646  PMID: 22179056
Lateral septum; Medial preoptic area; Alarm call; Anti-predator display; Black-capped chickadee
19.  Species differences in the relative densities of D1-like and D2-like dopamine receptor subtypes in the Japanese quail and rats: An in vitro quantitative receptor autoradiography study 
Brain, behavior and evolution  2009;73(2):81-90.
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.
PMCID: PMC3522861  PMID: 19321949
dopamine; autoradiography; apomorphine; male sexual behavior; bird
20.  On the Perception of Speech Sounds as Biologically Significant Signals1,2 
Brain, behavior and evolution  1979;16(5-6):330-350.
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.
PMCID: PMC3512094  PMID: 399200
Speech perception; Synthetic speech; Identification; Discrimination; Species-specific acoustic signals; Perceptual development; Feature detectors; Perceptual constancy; Speech mode
21.  Brain Transcriptomic Response of Threespine Sticklebacks to Cues of a Predator 
Brain, Behavior and Evolution  2011;77(4):270-285.
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.
PMCID: PMC3182040  PMID: 21677424
Neurogenomics; Stress; Predation; Microarray; Gene expression; Gasterosteus aculeatus
22.  Social Status and Sex Effects on Neural Morphology in Damaraland Mole-Rats, Fukomys damarensis 
Brain, Behavior and Evolution  2011;77(4):291-298.
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.
PMCID: PMC3182041  PMID: 21701152
Bed nucleus of the stria terminalis; Damaraland mole-rat; Medial amygdala; Naked mole-rat; Onuf's nucleus; Paraventricular nucleus; Sex difference; Social status
23.  All Rodents Are Not the Same: A Modern Synthesis of Cortical Organization 
Brain, Behavior and Evolution  2011;78(1):51-93.
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.
PMCID: PMC3182045  PMID: 21701141
Rats; Mice; Somatosensory cortex; Visual cortex; Auditory cortex; Motor cortex; Evolution
24.  Development of Tectal Connectivity across Metamorphosis in the Bullfrog (Rana catesbeiana) 
Brain, Behavior and Evolution  2011;76(3-4):226-247.
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.
PMCID: PMC3202948  PMID: 21266803
Medial septum; Metamorphosis; Midbrain; Multisensory convergence; Nucleus isthmi; Optic tectum; Tadpole; Thalamus
25.  A Potential Role for Glucose Transporters in the Evolution of Human Brain Size 
Brain, Behavior and Evolution  2011;78(4):315-326.
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.
PMCID: PMC3237107  PMID: 21986508
Glucose; Transporters; Brain; Evolution; Primates

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