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1.  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
2.  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
3.  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
4.  How Brains Are Built: Genetics and Evolution 
Brain, behavior and evolution  2013;81(2):71-73.
PMCID: PMC3632431  PMID: 23466525
5.  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
6.  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
7.  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
8.  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
9.  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
10.  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
11.  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
12.  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
13.  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
14.  Bigger Brains or Bigger Nuclei? Regulating the Size of Auditory Structures in Birds 
Brain, Behavior and Evolution  2004;63(3):169-180.
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.
PMCID: PMC3269630  PMID: 14726625
Evolution; Auditory; Neuronal computation; Birds; Allometry
15.  Plasticity of Auditory Medullary-Midbrain Connectivity across Metamorphic Development in the Bullfrog, Rana catesbeiana 
Brain, Behavior and Evolution  2006;69(1):1-19.
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.
PMCID: PMC3257804  PMID: 16912473
Tadpoles; Anurans; Vestibular nucleus complex; Dorsal medullary nucleus; Superior olivary complex; Torus semicircularis; Lipophilic dyes; PHA-L; Cholera toxin; Metamorphosis
16.  Developmental and Regional Patterns of GAP-43 Immunoreactivity in a Metamorphosing Brain 
Brain, Behavior and Evolution  2008;71(4):247-262.
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.
PMCID: PMC3257825  PMID: 18431052
Growth-associated protein 43; Plasticity; Metamorphosis; Bullfrog; Midbrain; Forebrain; Cranial nerves
17.  Cell Proliferation in the Forebrain and Midbrain of the Adult Bullfrog, Rana catesbeiana 
Brain, Behavior and Evolution  2007;71(1):41-53.
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.
PMCID: PMC3256745  PMID: 17878717
Cell proliferation; Neurogenesis; Gliogenesis; Amphibians; Bullfrog
18.  Phenotypic Specification of Hindbrain Rhombomeres and the Origins of Rhythmic Circuits in Vertebrates 
Brain, behavior and evolution  1997;50(Suppl 1):3-16.
This essay considers the ontogeny and phylogeny of the cranial neural circuitry producing rhythmic behaviors in vertebrates. These behaviors are characterized by predictable temporal patterns established by a neuronal network variously referred to as either a pacemaker, neural oscillator or central pattern generator. Comparative vertebrate studies have demonstrated that the embryonic hindbrain is divided into segmented compartments called rhombomeres, each of which gives rise to a distinct complement of cranial motoneurons and, as yet, unidentified populations of interneurons. We now propose that novel rhythmic circuits were innovations associated with the adoption of cardiac and respiratory pumps during the protochordate-vertebrate transition. We further suggest that the pattern-generating circuits of more recent innovations, such as the vocal, electromotor and extraocular systems, have originated from the same Hox gene-specified compartments of the embryonic hindbrain (rhombomeres 7–8) that gave rise to rhythmically active cardiac and respiratory circuits. Lastly, we propose that the capability for pattern generation by neurons originating from rhombomeres 7 and 8 is due to their electroresponsive properties producing pacemaker oscillations, as best typified by the inferior olive which also has origins from these same hindbrain compartments and has been suggested to establish rhythmic oscillations coupled to sensorimotor function throughout the neuraxis of vertebrates.
PMCID: PMC3023276  PMID: 9217990
Rhombomeres; Hindbrain; Hox genes; Pacemaker; Oscillator; Vocalization; Electromotor; Oculomotor; Inferior olive; Cerebellum; Teleost
19.  Distribution of 2-[125I]iodomelatonin Binding in the Brain of Mexican Free-Tailed Bats (Tadarida brasiliensis) 
Brain, behavior and evolution  2009;73(1):16-25.
The neurohormone melatonin is an important signal for both time of day and time of year in many seasonally breeding animals. High densities of melatonin receptors have been found in the suprachiasmatic nucleus, median eminence, and the pituitary gland in almost all mammals investigated so far, and lower densities of melatonin receptors have also been localized to other brain regions varying in a species-specific fashion. Because species-specific differences in receptor distributions have been correlated with differences in behavior and ecology, a comparative study of how melatonin receptors are distributed in vertebrate brains can be useful to the understanding of the functional organization of neural circuits controlling daily and seasonal behaviors. In this study, we localized and characterized melatonin binding sites in the brain of the Mexican free-tailed bat (Tadarida brasiliensis) using in vitro autoradiography with 2-[125I]iodomelatonin. Tadarida brasiliensis is a nocturnal insectivorous mammal that seasonally migrates, reproduces once a year, and exhibits documented sexual dimorphisms in seasonal reproductive behaviors, most notably in courtship vocalizations. Prominent 2-[125I]iodomelatonin binding was found in the median eminence, suprachiasmatic nuclei, and hippocampus, similar to that observed in other mammals. High densities of binding were also localized to structures of the basal ganglia, including the caudate nucleus, putamen, and nucleus accumbens, a feature commonly observed in songbirds but not in mammals. Saturation analysis indicated that the observed binding sites had an affinity for melatonin typical of the binding properties for the Mel1a receptor subtype. We conclude that melatonin receptor distributions in the Mexican free-tailed bat brain appear to show similarities with the reproductive and circadian systems of other mammals and the basal ganglia of songbirds.
PMCID: PMC2825557  PMID: 19223684
Bats; Basal ganglia; Hippocampus; Melatonin; Suprachiasmatic nucleus
20.  Early ontogeny of the olfactory organ in a basal actinopterygian fish: Polypterus 
Brain, behavior and evolution  2009;73(4):259-272.
The present study employed light and electron microscopic methods to investigate the ontogenetic origin of the olfactory organ in bichirs (Cladistia: Polypteridae) and explore its evolution among osteichthyans. In former studies we demonstrated that in teleosts a subepidermal layer gives rise to the olfactory placode which in turn builds all types of olfactory cells (basal, receptor, supporting, ciliated non-sensory cells). In contrast, the olfactory placodes in sturgeons (Chondrostei: Acipenseridae) as well as in the clawed frog Xenopus laevis (Anura: Pipidae) originate from two different layers. Receptor neurons derive from cells of the subepidermal (sensory) layer and supporting cells from epidermal cells. As sturgeons and amphibians in some characters show a more primitive condition than teleosts, we extended our study to Polypterus to allow for an approach at the basic osteichthyan pattern. In Polypterus, an internal lumen occurs in early ontogenetic stages surrounded by the epithelium of the olfactory placode. Two different populations of supporting cells follow one another: a primary population derives from the subepidermal layer. Later supporting cells develop from epidermal cells by transdifferentiation. The primary opening of the internal lumen to the exterior develops by invagination from the epidermal surface and simultaneously by a counter-directed process of cell dissociation and fragmentation inside the olfactory placode. Our results indicate the following features to be plesiomorphic actinopterygian character states: The primary olfactory pit (prospective olfactory cavity) is formed by invagination of the epidermal and the subepidermal layer (as in Acipenser and Xenopus). The incurrent and excurrent nostrils derive from a single primary opening which elongates and is then separated by an epidermal bridge into the two external openings (as in Acipenser and many teleosts). The olfactory epithelium derives from an epidermal and a subepidermal layer (as in Acipenser and Xenopus). Apomorphic (derived actinopterygian) features are: (1) an internal lumen as primordium of the future olfactory chamber; (2) a subepidermal layer gives rise to the olfactory epithelium and its constituents (Polypterus and teleosts). As to the origin of the olfactory supporting cells in Polypterus we assume a combination of plesiomorphic and apomorphic characters. We conclude that Acipenser and Xenopus exhibit the most widely distributed features among basal osteognathostomes and thus ancestral character states in the development of the olfactory organs.
PMCID: PMC2746032  PMID: 19590178
Actinopterygii; Cladistia; Olfactory Placode; Ontogeny; Phylogeny; Ultrastructure
21.  Exploring the Origins of the Human Brain through Molecular Evolution 
Brain, behavior and evolution  2008;72(2):168-177.
The emergence of the human brain is one of evolution’s most compelling mysteries. With its singular importance and astounding complexity, understanding the forces that gave rise to the human brain is a major undertaking. Recently, the identification and publication of the complete genomic sequence of humans, mice, chimpanzees, and macaques has allowed for large-scale studies looking for the genic substrates of this natural selection. These investigations into positive selection, however, have generally produced incongruous results. Here we consider some of these studies and their differences in methodologies with an eye towards how they affect the results. We also clarify the strengths and weaknesses of each of these approaches and discuss how these can be synthesized to develop a more complete understanding of the genetic correlates behind the human brain and the selective events that have acted upon them.
PMCID: PMC2700753  PMID: 18836262
Hominid; Primate; Human evolution; Brain evolution; Neurogenetics; Molecular evolution
22.  Auditory sensitivity of an acoustic parasitoid (Emblemasoma sp., Sarcophagidae, Diptera) and the calling behavior of potential hosts 
Brain, behavior and evolution  2008;72(1):16-26.
Using field broadcasts of model male calling songs, we tested whether Tibicen pruinosa and T. chloromera (Homoptera: Cicadidae) are candidate hosts for acoustic parasitoid flies. The model calling song of T. pruinosa attracted 90% of the flies (Sarcophagidae: Emblemasoma sp.; all larvapositing females) when broadcast simultaneously with the model T. chloromera song, a phonotactic bias reconfirmed in single song playbacks. In paired broadcasts of model T. pruinosa songs with different relative amplitudes (3 dB or 6 dB), significantly more flies were attracted to the more powerful song, a result consistent with the responses predicted by a model proposed by Forrest and Raspet [1994]. Using intracellular recordings and dye injections, we characterized the sensitivity of auditory units in sound-trapped flies. Intracellular recordings from six auditory units (5 interneurons, 1 afferent) revealed best sensitivity for frequencies near 3-4 kHz, matching the predominant spectral components of the calling songs of both species of cicada. Interestingly, although flies could be attracted to T. pruinosa broadcasts throughout the day, hourly censuses of singing males revealed that calling occurred exclusively at dusk. Furthermore, the duration of the dusk chorus in T. pruinosa was significantly shorter than the midday chorus of the less attractive song of T. chloromera. We propose that the tight temporal aggregation of the dusk chorus time could function to reduce risk from attracted parasitoids.
PMCID: PMC2644656  PMID: 18560209
Cicada; Diel Behavior; Parasitoid; Cricket; Chorus; Tibicen; Ormia; Emblemasoma; phonotaxis; interneuron; frequency tuning
23.  The Eye of the Laboratory Mouse Remains Anatomically Adapted for Natural Conditions 
Brain, behavior and evolution  2005;67(1):39-52.
Evolutionary effects of domestication have been demonstrated for several body systems, including the eye, and for several vertebrate species, including the mouse. Given the importance of the laboratory mouse to vision science, we wished to determine whether the anatomical and histological features of the eyes of laboratory mice are distinct from those of their naturally adapted, wild counterparts. We measured dimensions and masses of whole eyes and lenses from a wild population plus three inbred strains (C57BL/6J, NZB/BINJ, and DBA/1J) of the house house, Mus musculus, as well as wild and outbred laboratory-domesticated stock of the deer mouse, Peromyscus maniculatus. Histological preparations from these eyes were used to determine outer nuclear layer thickness, linear density of the ganglion cell layer, and for indirect immunofluorescence evaluation of cone opsin expression. For all of these traits, no statistically significant differences were found between any laboratory strain and its wild counterpart. The evolutionary effects of domestication of mice therefore do not include changes to the eye in any variable measured, supporting the continued use of this animal as a model for a naturally adapted visual system.
PMCID: PMC2582157  PMID: 16219997
Mouse; Eye; Photoreceptor; Ganglion cell; Evolution; Domestication; Vision; Mammal
24.  Social Signals Regulate Gonadotropin-Releasing Hormone Neurons in the Green Treefrog 
Brain, behavior and evolution  2004;65(1):26-32.
Animals coordinate their physiological state with external cues to appropriately time reproduction. These external cues exert effects through influences on the gonadotropin-releasing hormone neurons (GnRH), at the apex of the hypothalamus-pituitary-gonad (HPG) axis. In green treefrogs, mating calls are important regulators of reproductive behavior and physiology. Reception of mating calls causes an increase in androgen levels, and androgens promote the production of mating calls, demonstrating a mutual influence between the communication and endocrine systems. In order to investigate the central nervous system correlates of social regulation of the HPG axis in green treefrogs, we exposed males to a mating chorus or a control stimulus (tones), counted the resulting number of septopreoptic GnRH-immunoreactive cells (GnRH-ir), and measured changes in plasma androgens. We found that reception of the mating chorus caused an increase in the number of GnRH-ir cells. As previously shown, we also found that the reception of the mating chorus resulted in higher androgen levels, suggesting that the higher GnRH-ir cell number represents increased GnRH production and release. We suggest that mating calls are an important supplementary cue that promotes GnRH production and release within the context of GnRH regulation by seasonal cues. Previous studies have proposed a neuroanatomical link between the anuran auditory system and GnRH neurons. Our results demonstrate a functional role for this proposed sensory-endocrine circuit, and show for the first time an influence of acoustic signals on GnRH neurons.
PMCID: PMC2581501  PMID: 15489562
GnRH; Amphibian; Treefrog; Acoustic communication; Androgens; Supplementary reproductive cue
25.  Characterization of the Shark Myelin Po Protein 
Brain, behavior and evolution  2008;72(1):48-58.
Myelin, the insulating sheath made by extensive plasma membrane wrappings is dependent on the presence of highly adhesive molecules that keep the two sides of the membrane in tight contact. The Po glycoprotein (Po) is the major component of the peripheral nervous system (PNS) myelin of mammals. The exact role that Po protein has played in the evolution of myelin is still unclear, but several phylogenetic observations point to it as a crucial component in the development of myelin as a multi-lamellar membrane structure. Sharks, which appeared in evolution about 400 million years ago, are the first fully myelinated organisms. In this study we set out to investigate the expression pattern of shark myelin Po as a way of understanding how it might have played a role in the evolution of myelin in the central nervous system. We found that shark have more than two isoforms (32, 28 and 25kD), and that some of these might not be fully functional because they lack the domains known for Po homophilic adhesion.
PMCID: PMC2574774  PMID: 18635929

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