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1.  Is male rhesus macaque red color ornamentation attractive to females? 
Behavioral ecology and sociobiology  2014;68(7):1215-1224.
Male sexually-selected traits can evolve through different mechanisms: conspicuous and colorful ornaments usually evolve through inter-sexual selection, while weapons usually evolve through intra-sexual selection. Male ornaments are rare among mammals in comparison to birds, leading to the notion that female mate choice generally plays little role in trait evolution in this taxon. Supporting this view, when ornaments are present in mammals they typically indicate social status and are products of male-male competition. This general mammalian pattern, however, may not apply to rhesus macaques (Macaca mulatta). Males of this species display conspicuous skin coloration, but this expression is not correlated to dominance rank, and is therefore unlikely to have evolved due to male-male competition. Here, we investigate whether male color expression influences female proceptivity towards males in the Cayo Santiago free-ranging rhesus macaque population. We collected face images of 24 adult males varying in dominance rank and age at the peak of the mating season, and modeled these to rhesus macaque visual perception. We also recorded female socio-sexual behaviors towards these males. Results show that dark red males received more sexual solicitations, by more females, than pale pink ones. Together with previous results, our study suggests that male color ornaments are more likely to be a product of inter- rather than intra-sexual selection. This may especially be the case in rhesus macaques due to the particular characteristics of male-male competition in this species.
PMCID: PMC4167843  PMID: 25246728
Ornaments; sexual selection; female mate choice; sexual skin; color; anthropoid primates
2.  Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior 
Behavioral ecology and sociobiology  2013;67(9):1457-1469.
The past decade has seen an increasing shift in animal communication towards more studies that incorporate aspects of signaling in multiple modalities. Although nonhuman primates are an excellent group for studying the extent to which different aspects of condition may be signaled in different modalities, and how such information may be integrated during mate choice, very few studies of primate species have incorporated such analyses. Here, we present data from free-ranging male rhesus macaques on sex skin coloration (modeled to receiver perception), bark vocal signals, androgen levels, morphometric variables, dominance status, and female mate choice. We show that, consistent with data on females, most intra- and interindividual variation in sex skin appearance occurs in luminance rather than color. Sex skin luminance was significantly correlated across different skin regions. Sex skin luminance did not correlate with the majority of bark parameters, suggesting the potential for the two signals to convey different information. Sex skin appearance was not related to androgen levels although we found some evidence for links between androgen levels and bark parameters, several of which were also related to morphometric variables. We found no evidence that either signal was related to male dominance rank or used in female mate choice, though more direct measures of female proceptive behavior are needed. Overall, the function of male sex skin coloration in this species remains unclear. Our study is among the first nonhuman primate studies to incorporate measurements of multiple signals in multiple modalities, and we encourage other authors to incorporate such analyses into their work.
PMCID: PMC4084859  PMID: 25013266
Coloration; Luminance; Vocal signals; Multimodal; Primate; Rhesus macaques
3.  Incidence of chromosomal mosaicism in morphologically normal non-human primate preimplantation embryos 
Fertility and sterility  2009;93(8):2545-2550.
To establish the exact rates of chromosomal mosaicism in morphologically normal rhesus macaque embryos by determining the chromosomal complement of all blastomeres.
Retrospective rhesus monkey IVF study.
Academic laboratory and Primate Research Center.
Young fertile rhesus macaque females.
Morphologically normal, in vitro produced rhesus macaque embryos were dissociated and cytogenetically assessed using a 5-color fluorescent in situ hybridization assay developed for rhesus macaque chromosomes homologous to human chromosomes 13, 16, 18, X and Y.
Main Outcome Measure(s)
The incidence and extent of chromosomal mosaicism in rhesus macaque preimplantation embryos.
Seventy-seven preimplantation embryos, displaying normal morphology and development, from 17 young rhesus macaque females were analyzed. Overall, 39 embryos (50.6%) were normal, 14 embryos (18.2%) were completely abnormal and 24 embryos were mosaic (31.2%). Of the 226 blastomeres analyzed in the mosaic group, 110 blastomeres (48.7%) were normal.
The observed rate of mosaicism in good quality rhesus embryos resembles previously-documented frequencies in poor-quality human preimplantation embryos. A high incidence of mosaicism may limit the diagnostic accuracy of preimplantation genetic diagnosis.
PMCID: PMC3150520  PMID: 19732891
Mosaicism; embryos; monkey; non-human primate; aneuploidy; FISH
4.  Chromosomal instability in rhesus macaque preimplantation embryos 
Fertility and sterility  2008;91(4):1230-1237.
To establish a relevant animal model to systematically investigate chromosomal instability in human oocytes and preimplantation embryos.
Prospective rhesus monkey IVF study.
Academic laboratory, Oregon National Primate Research Center and Caribbean Primate Research Center.
Young Rhesus macaque females.
In vitro produced (IVP) entire rhesus macaque preimplantation embryos were cytogenetically assessed using a 5-color fluorescent in situ hybridization (FISH) assay developed for rhesus macaque chromosomes homologous to human chromosomes 13, 16, 18, X and Y, using human bacterial artificial chromosome (BAC) probes.
Main Outcome Measure(s)
Chromosomal abnormality rates in preimplantation embryos from young rhesus macaque females were established.
Fifty preimplantation embryos, displaying good morphology and normal development, from 11 young rhesus macaque females were analyzed. Overall, 27 embryos (54%) were normal, 11 embryos (22%) mosaic, 3 embryos (6%) chaotic, 2 embryos (4%) aneuploid, 3 embryos (6%) haploid and 4 embryos (8%) triploid.
These data indicate that IVP rhesus macaque and human preimplantation embryos exhibit similar numerical chromosomal aberrations. Rhesus macaques appear to be a suitable animal model for investigating the origin of chromosomal instability observed in human preimplantation embryos.
PMCID: PMC3082460  PMID: 18440514
Aneuploidy; ART; Cytogenetics; Embryo; FISH; IVF; Non-human primate; PGD
5.  Estimating rice chlorophyll content and leaf nitrogen concentration with a digital still color camera under natural light 
Plant Methods  2014;10(1):36.
The color of crop leaves is closely correlated with nitrogen (N) status and can be quantified easily with a digital still color camera and image processing software. The establishment of the relationship between image color indices and N status under natural light is important for crop monitoring and N diagnosis in the field. In our study, a digital still color camera was used to take pictures of the canopies of 6 rice (Oryza sativa L.) cultivars with N treatments ranging from 0 to 315 kg N ha-1 in the field under sunny and overcast conditions in 2010 and 2011, respectively.
Significant correlations were observed between SPAD readings, leaf N concentration (LNC) and 13 image color indices calculated from digital camera images using three color models: RGB, widely used additive color model; HSV, a cylindrical-coordinate similar to the human perception of colors; and the L*a*b* system of the International Commission on Illumination. Among these color indices, the index b*, which represents the visual perception of yellow-blue chroma, has the closest linear relationship with SPAD reading and LNC. However, the relationships between LNC and color indices were affected by the developmental phase. Linear regression models were used to predict LNC and SPAD from color indices and phasic development. After that, the models were validated with independent data. Generally, acceptable performance and prediction were found between the color index b*, SPAD reading and LNC with different cultivars and sampling dates under different natural light conditions.
Our study showed that digital color image analysis could be a simple method of assessing rice N status under natural light conditions for different cultivars and different developmental stages.
Electronic supplementary material
The online version of this article (doi:10.1186/1746-4811-10-36) contains supplementary material, which is available to authorized users.
PMCID: PMC4236477  PMID: 25411579
Digital still color camera; Leaf color; Image processing technology; Natural light; Nitrogen; Rice
6.  Color accuracy of commercial digital cameras for use in dentistry 
The use of calibrated, commercial digital cameras for dental applications is promising. The color accuracy of various calibration models were evaluated as applied to three commercial digital cameras for use in dental color matching.
CIE LAB values of 264 color patches and 65 shade tabs were measured with a spectroradiometer. Digital images of the samples were taken with the Nikon D100, Canon D60 and Sigma SD9 cameras. Four regression models were formulated from the color patch CIE LAB and the digital image values. Shade tab CIE LAB colors were predicted by applying the digital image values into the calibration models and were compared to the measured CIE LAB values. The Wilcoxon Rank-Sum test determined if the 12 camera/calibration models differed significantly from the color measurement setup.
Every camera/calibration model (ΔE’s ranging from 1.79 to 5.25) showed a statistically significant difference from the color measurement setup.
Commercial SLR digital cameras when combined with the appropriate calibration protocols showed potential for use in the color replication process of clinical dentistry.
PMCID: PMC1808262  PMID: 16198403
Digital cameras; Calibration models; Color measurement; Translucent material
7.  Functional diversity in the color vision of cichlid fishes 
BMC Biology  2010;8:133.
Color vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed.
To examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes.
Our study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.
PMCID: PMC2988715  PMID: 21029409
8.  The Heterozygote Superiority Hypothesis for Polymorphic Color Vision Is Not Supported by Long-Term Fitness Data from Wild Neotropical Monkeys 
PLoS ONE  2014;9(1):e84872.
The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.
PMCID: PMC3880319  PMID: 24404195
9.  The Verriest Lecture: Color lessons from space, time, and motion 
The appearance of a chromatic stimulus depends on more than the wavelengths composing it. The scientific literature has countless examples showing that spatial and temporal features of light influence the colors we see. Studying chromatic stimuli that vary over space, time or direction of motion has a further benefit beyond predicting color appearance: the unveiling of otherwise concealed neural processes of color vision. Spatial or temporal stimulus variation uncovers multiple mechanisms of brightness and color perception at distinct levels of the visual pathway. Spatial variation in chromaticity and luminance can change perceived three-dimensional shape, an example of chromatic signals that affect a percept other than color. Chromatic objects in motion expose the surprisingly weak link between the chromaticity of objects and their physical direction of motion, and the role of color in inducing an illusory motion direction. Space, time and motion – color’s colleagues – reveal the richness of chromatic neural processing.
PMCID: PMC3492961  PMID: 22330398
10.  Traceable Calibration, Performance Metrics, and Uncertainty Estimates of Minirhizotron Digital Imagery for Fine-Root Measurements 
PLoS ONE  2014;9(11):e112362.
Even though fine-root turnover is a highly studied topic, it is often poorly understood as a result of uncertainties inherent in its sampling, e.g., quantifying spatial and temporal variability. While many methods exist to quantify fine-root turnover, use of minirhizotrons has increased over the last two decades, making sensor errors another source of uncertainty. Currently, no standardized methodology exists to test and compare minirhizotron camera capability, imagery, and performance. This paper presents a reproducible, laboratory-based method by which minirhizotron cameras can be tested and validated in a traceable manner. The performance of camera characteristics was identified and test criteria were developed: we quantified the precision of camera location for successive images, estimated the trueness and precision of each camera's ability to quantify root diameter and root color, and also assessed the influence of heat dissipation introduced by the minirhizotron cameras and electrical components. We report detailed and defensible metrology analyses that examine the performance of two commercially available minirhizotron cameras. These cameras performed differently with regard to the various test criteria and uncertainty analyses. We recommend a defensible metrology approach to quantify the performance of minirhizotron camera characteristics and determine sensor-related measurement uncertainties prior to field use. This approach is also extensible to other digital imagery technologies. In turn, these approaches facilitate a greater understanding of measurement uncertainties (signal-to-noise ratio) inherent in the camera performance and allow such uncertainties to be quantified and mitigated so that estimates of fine-root turnover can be more confidently quantified.
PMCID: PMC4229195  PMID: 25391023
11.  Do common mechanisms of adaptation mediate color discrimination and appearance? Uniform backgrounds 
Color vision is useful for detecting surface boundaries and identifying objects. Are the signals used to perform these two functions processed by common mechanisms, or has the visual system optimized its processing separately for each task? We measured the effect of mean chromaticity and luminance on color discriminability and on color appearance under well-matched stimulus conditions. In the discrimination experiments, a pedestal spot was presented in one interval and a pedestal + test in a second. Observers indicated which interval contained the test. In the appearance experiments, observers matched the appearance of test spots across a change in background. We analyzed the data using a variant of Fechner's proposal, that the rate of apparent stimulus change is proportional to visual sensitivity. We found that saturating visual response functions together with a model of adaptation that included multiplicative gain control and a subtractive term accounted for data from both tasks. This result suggests that effects of the contexts we studied on color appearance and discriminability are controlled by the same underlying mechanism.
PMCID: PMC1815483  PMID: 16277280
12.  Facial Musculature in the Rhesus Macaque (Macaca mulatta): Evolutionary and Functional Contexts with Comparisons to Chimpanzees and Humans 
Journal of anatomy  2009;215(3):320-334.
Facial expression is a common mode of visual communication in mammals but especially so in primates. Rhesus macaques (Macaca mulatta) have a well-documented facial expression repertoire that is controlled by the facial/mimetic musculature as in all mammals. However, little is known about the musculature itself and how it compares to those of other primates. Here we present a detailed description of the facial musculature in rhesus macaques in behavioral, evolutionary, and comparative contexts. Foramlin-fixed faces from six adult male specimens were dissected using a novel technique. The morphology, attachments, three-dimensional relationships, and variability of muscles were noted and compared with chimpanzees (Pan troglodytes) and with humans. Results showed that there was a greater number of facial muscles in rhesus macaques than previously described (24) including variably present (and previously unmentioned) zygomaticus minor, levator labii superioris alaeque nasi, depressor septi, anterior auricularis, inferior auricularis, and depressor supercilii muscles. Facial muscles of the rhesus macaque were very similar to those in chimpanzees and in humans but M. mulatta did not possess a risorius muscle. These results support previous studies that describe a highly graded and intricate facial expression repertoire in rhesus macaques. Furthermore, these results indicate that phylogenetic position is not the primary factor governing structure of primate facial musculature and that other factors such as social behavior are probably more important. Results from the present study may provide valuable input to both biomedical studies that use rhesus macaques as a model for human disease and disorder that includes assessment of facial movement and studies into the evolution of primate societies and communication.
PMCID: PMC2750044  PMID: 19563473
macaque; facial muscle; mimetic; chimpanzee; evolution; facial expression; primate
13.  Color opponent receptive fields self-organize in a biophysical model of visual cortex via spike-timing dependent plasticity 
Although many computational models have been proposed to explain orientation maps in primary visual cortex (V1), it is not yet known how similar clusters of color-selective neurons in macaque V1/V2 are connected and develop. In this work, we address the problem of understanding the cortical processing of color information with a possible mechanism of the development of the patchy distribution of color selectivity via computational modeling. Each color input is decomposed into a red, green, and blue representation and transmitted to the visual cortex via a simulated optic nerve in a luminance channel and red–green and blue–yellow opponent color channels. Our model of the early visual system consists of multiple topographically-arranged layers of excitatory and inhibitory neurons, with sparse intra-layer connectivity and feed-forward connectivity between layers. Layers are arranged based on anatomy of early visual pathways, and include a retina, lateral geniculate nucleus, and layered neocortex. Each neuron in the V1 output layer makes synaptic connections to neighboring neurons and receives the three types of signals in the different channels from the corresponding photoreceptor position. Synaptic weights are randomized and learned using spike-timing-dependent plasticity (STDP). After training with natural images, the neurons display heightened sensitivity to specific colors. Information-theoretic analysis reveals mutual information between particular stimuli and responses, and that the information reaches a maximum with fewer neurons in the higher layers, indicating that estimations of the input colors can be done using the output of fewer cells in the later stages of cortical processing. In addition, cells with similar color receptive fields form clusters. Analysis of spiking activity reveals increased firing synchrony between neurons when particular color inputs are presented or removed (ON-cell/OFF-cell).
PMCID: PMC3950416  PMID: 24659956
brain modeling; visual cortex; neocortex; color; color selectivity; self-organizing color maps; self-organizing feature maps; STDP
14.  Sex and vision II: color appearance of monochromatic lights 
Because cerebral cortex has a very large number of testosterone receptors, we examined the possible sex differences in color appearance of monochromatic lights across the visible spectrum. There is a history of men and women perceiving color differently. However, all of these studies deal with higher cognitive functions which may be culture-biased. We study basic visual functions, such as color appearance, without reference to any objects. We present here a detailed analysis of sex differences in primary chromatic sensations.
We tested large groups of young adults with normal vision, including spatial and temporal resolution, and stereopsis. Based on standard color-screening and anomaloscope data, we excluded all color-deficient observers. Stimuli were equi-luminant monochromatic lights across the spectrum. They were foveally-viewed flashes presented against a dark background. The elicited sensations were measured using magnitude estimation of hue and saturation. When the only permitted hue terms are red (R) yellow (Y), green (G), blue (B), alone or in combination, such hue descriptions are language-independent and the hue and saturation values can be used to derive a wide range of color-discrimination functions.
There were relatively small but clear and significant, differences between males and females in the hue sensations elicited by almost the entire spectrum. Generally, males required a slightly longer wavelength to experience the same hue as did females. The spectral loci of the unique hues are not correlated with anomaloscope matches; these matches are directly determined by the spectral sensitivities of L- and M-cones (genes for these cones are on the X-chromosomes). Nor are there correlations between loci of pairs of unique hues (R, Y, G, B). Wavelength-discrimination functions derived from the scaling data show that males have a broader range of poorer discrimination in the middle of the spectrum. The precise values for all the data depend on whether Newtonian or Maxwellian optics were used, but the sex differences were the same for both optical systems.
As with our associated paper on spatio-temporal vision, there are marked sex differences in color vision. The color-appearances we measured are determined by inputs from thalamic neurons (LGN) to individual neurons in primary visual cortex. This convergence from LGN to cortex is guided by the cortex during embryogenesis. We hypothesize that testosterone plays a major role, somehow leading to different connectivities for males and females: color appearance requires a re-combination and re-weighting of neuronal inputs from the LGN to the cortex, which, as we show, depends on the sex of the participant.
PMCID: PMC3483194  PMID: 22943488
15.  Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish 
PLoS ONE  2014;9(7):e101497.
The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.
PMCID: PMC4079317  PMID: 24987856
In 1993, DeValois and DeValois proposed a “multi-stage color model” to explain how the cortex is ultimately able to deconfound the responses of neurons receiving input from three cone types in order to produce separate red-green and blue-yellow systems, as well as segregate luminance percepts (black-white) from color. This model extended the biological implementation of Hurvich and Jameson’s Opponent-Process Theory of color vision, a two-stage model encompassing the three cone types combined in a later opponent organization, which has been the accepted dogma in color vision. DeValois’ model attempts to satisfy the long-remaining question of how the visual system separates luminance information from color, but what are the cellular mechanisms that establish the complicated neural wiring and higher-order operations required by the Multi-stage Model? During the last decade and a half, results from molecular biology have shed new light on the evolution of primate color vision, thus constraining the possibilities for the visual circuits. The evolutionary constraints allow for an extension of DeValois' model that is more explicit about the biology of color vision circuitry, and it predicts that human red-green colorblindness can be cured using a retinal gene therapy approach to add the missing photopigment, without any additional changes to the post-synaptic circuitry.
PMCID: PMC3044922  PMID: 20238067
17.  Appearance-Based Multimodal Human Tracking and Identification for Healthcare in the Digital Home 
Sensors (Basel, Switzerland)  2014;14(8):14253-14277.
There is an urgent need for intelligent home surveillance systems to provide home security, monitor health conditions, and detect emergencies of family members. One of the fundamental problems to realize the power of these intelligent services is how to detect, track, and identify people at home. Compared to RFID tags that need to be worn all the time, vision-based sensors provide a natural and nonintrusive solution. Observing that body appearance and body build, as well as face, provide valuable cues for human identification, we model and record multi-view faces, full-body colors and shapes of family members in an appearance database by using two Kinects located at a home's entrance. Then the Kinects and another set of color cameras installed in other parts of the house are used to detect, track, and identify people by matching the captured color images with the registered templates in the appearance database. People are detected and tracked by multisensor fusion (Kinects and color cameras) using a Kalman filter that can handle duplicate or partial measurements. People are identified by multimodal fusion (face, body appearance, and silhouette) using a track-based majority voting. Moreover, the appearance-based human detection, tracking, and identification modules can cooperate seamlessly and benefit from each other. Experimental results show the effectiveness of the human tracking across multiple sensors and human identification considering the information of multi-view faces, full-body clothes, and silhouettes. The proposed home surveillance system can be applied to domestic applications in digital home security and intelligent healthcare.
PMCID: PMC4179041  PMID: 25098207
home healthcare; human detection; human tracking; human identification
18.  The rhesus macaque is three times as diverse but more closely equivalent in damaging coding variation as compared to the human 
BMC Genetics  2012;13:52.
As a model organism in biomedicine, the rhesus macaque (Macaca mulatta) is the most widely used nonhuman primate. Although a draft genome sequence was completed in 2007, there has been no systematic genome-wide comparison of genetic variation of this species to humans. Comparative analysis of functional and nonfunctional diversity in this highly abundant and adaptable non-human primate could inform its use as a model for human biology, and could reveal how variation in population history and size alters patterns and levels of sequence variation in primates.
We sequenced the mRNA transcriptome and H3K4me3-marked DNA regions in hippocampus from 14 humans and 14 rhesus macaques. Using equivalent methodology and sampling spaces, we identified 462,802 macaque SNPs, most of which were novel and disproportionately located in the functionally important genomic regions we had targeted in the sequencing. At least one SNP was identified in each of 16,797 annotated macaque genes. Accuracy of macaque SNP identification was conservatively estimated to be >90%. Comparative analyses using SNPs equivalently identified in the two species revealed that rhesus macaque has approximately three times higher SNP density and average nucleotide diversity as compared to the human. Based on this level of diversity, the effective population size of the rhesus macaque is approximately 80,000 which contrasts with an effective population size of less than 10,000 for humans. Across five categories of genomic regions, intergenic regions had the highest SNP density and average nucleotide diversity and CDS (coding sequences) the lowest, in both humans and macaques. Although there are more coding SNPs (cSNPs) per individual in macaques than in humans, the ratio of dN/dS is significantly lower in the macaque. Furthermore, the number of damaging nonsynonymous cSNPs (have damaging effects on protein functions from PolyPhen-2 prediction) in the macaque is more closely equivalent to that of the human.
This large panel of newly identified macaque SNPs enriched for functionally significant regions considerably expands our knowledge of genetic variation in the rhesus macaque. Comparative analysis reveals that this widespread, highly adaptable species is approximately three times as diverse as the human but more closely equivalent in damaging variation.
PMCID: PMC3426462  PMID: 22747632
Rhesus macaque; Human; Single nucleotide polymorphism; Diversity; Comparative genomics
19.  Contrast enhanced ultrasound reveals real-time spatial changes in vascular perfusion during early implantation in the macaque uterus 
Fertility and sterility  2011;95(4):1316-1321.e3.
To use contrast enhanced ultrasound (CEU) to quantify blood flow in the macaque uterus during early pregnancy.
Prospective nonhuman primate study.
National Primate Research Center.
Naturally cycling female rhesus macaques (Macaca mulatta).
Female macaques were mated on days 11–14 of the cycle. Females were then imaged by CEU and Doppler ultrasound (DUS) once every 3 days from day 21 through day 39 of the fertile cycle.
Main Outcome Measures
Visualization and quantification of uterine vascular perfusion.
CEU identified the primary placental disc and underlying vessels ~2 days earlier than DUS was able to observe endometrial thickening. CEU revealed spatial differences in vascular perfusion between the endometrium, myometrium, and the endometrial-myometrial (junctional) zone. Myometrium displayed the highest rate of blood flow (>10 mL/min/g tissue). There was less blood flow in the endometrium and junctional zone (<3 mL/min/g). A brief fall in progesterone was observed during early implantation, which was correlated with reduced blood flow to all three uterine compartments, but did not reduce flow to the placenta.
CEU provides a sensitive, non-invasive method to assess vascular perfusion of the uterus during embryo implantation in macaques. We propose CEU as a new diagnostic tool to monitor vascular changes associated with early pregnancy in women.
PMCID: PMC3070443  PMID: 21316046
contrast enhanced ultrasound; Doppler ultrasound; endometrium; implantation; macaque; pregnancy; progesterone; uterus; vascular perfusion
20.  Characterization of color CRT display systems for monochrome applications 
Journal of Digital Imaging  1999;12(3):102-113.
Soft-copy presentation of medical images is becoming more and more important as medical imaging is strongly moving toward digital technology, and health care facilities are converting to filmless hospital and radiological information management. Although most medical images are monochrome, frequently they are displayed on color CRTs, particularly if general-purpose workstations or PCs are used for medical viewing. In the present report, general measurement and modeling procedures for the characterization of color CRT monitors for monochrome presentation are introduced. The contributions from the three color channels (red, green, and blue) are weighted according to the spectral sensitivity of the human eye for photopic viewing. The luminance behavior and the resolution capabilities of color CRT monitors are analyzed with the help of photometer and charge-coupled device (CCD) camera measurements. For the evaluation of spatial resolution, a two-dimensional Fourier analysis of special test images containing white noise (broadband response) is employed. A stage model for a color CRT monitor is developed to discuss the effects of scanning and dot sampling. Furthermore, display intrinsic veiling glare and reflectivity of typical color CRT monitors are measured and compared with those of monochrome CRT monitors. The developed methods and models allow one to describe the image quality aspects of color monitors if they are applied for medical monochrome image presentation. Particularly, because of the reduced luminance and dynamic range of color monitors, the calibration and control of their luminance curves is a very important task. For present color CRT monitors, 1,280×1,024 turns out to be an intrinsic limit for the displayable matrix of medical images.
PMCID: PMC3452435  PMID: 10461573
monitor characterization; color CRT monitors; soft-copy viewing; image quality
21.  Sex-Specific Heritability of Spontaneous Lipid Levels in an Extended Pedigree of Indian-Origin Rhesus Macaques (Macaca mulatta) 
PLoS ONE  2013;8(8):e72241.
The rhesus macaque is an important model for human atherosclerosis but genetic determinants of relevant phenotypes have not yet been investigated in this species. Because lipid levels are well-established and heritable risk factors for human atherosclerosis, our goal was to assess the heritability of lipoprotein cholesterol and triglyceride levels in a single, extended pedigree of 1,289 Indian-origin rhesus macaques. Additionally, because increasing evidence supports sex differences in the genetic architecture of lipid levels and lipid metabolism in humans and macaques, we also explored sex-specific heritability for all lipid measures investigated in this study. Using standard methods, we measured lipoprotein cholesterol and triglyceride levels from fasted plasma in a sample of 193 pedigreed rhesus macaques selected for membership in large, paternal half-sib cohorts, and maintained on a low-fat, low cholesterol chow diet. Employing a variance components approach, we found moderate heritability for total cholesterol (h2=0.257, P=0.032), LDL cholesterol (h2=0.252, P=0.030), and triglyceride levels (h2=0.197, P=0.034) in the full sample. However, stratification by sex (N=68 males, N=125 females) revealed substantial sex-specific heritability for total cholesterol (0.644, P=0.004, females only), HDL cholesterol (0.843, P=0.0008, females only), VLDL cholesterol (0.482, P=0.018, males only), and triglyceride levels (0.705, P=0.001, males only) that was obscured or absent when sexes were combined in the full sample. We conclude that genes contribute to spontaneous variation in circulating lipid levels in the Indian-origin rhesus macaque in a sex-specific manner, and that the rhesus macaque is likely to be a valuable model for sex-specific genetic effects on lipid risk factors for human atherosclerosis. These findings are a first-ever report of heritability for cholesterol levels in this species, and support the need for expanded analysis of these traits in this population.
PMCID: PMC3738547  PMID: 23951301
22.  Toward Quantifying the Aesthetic Outcomes of Breast Cancer Treatment: Comparison of Clinical Photography and Colorimetry 
Rationale, aims and objectives
Scarring is a significant cause of dissatisfaction for women who undergo breast surgery. Scar tissue may be clinically distinguished from normal skin by aberrant color, rough surface texture, increased thickness (hypertrophy), and firmness. Colorimeters or spectrophotometers can be used to quantitatively assess scar color, but they require direct patient interaction and can cost thousands of dollars By comparison, digital photography is already in widespread use to document clinical outcomes and requires less patient interaction. Thus, assessment of scar coloration by digital photography is an attractive alternative. The goal of this study was to compare color measurements obtained by digital photography and colorimetry.
Agreement between photographic and colorimetric measurements of color were evaluated. Experimental conditions were controlled by performing measurements on artificial scars created by a makeup artist. The colorimetric measurements of the artificial scars were compared to those reported in the literature for real scars in order to confirm the validity of this approach. We assessed the agreement between the colorimetric and photographic measurements of color using a hypothesis test for equivalence, the intra-class correlation coefficient (ICC), and the Bland-Altman method.
Overall, good agreement was obtained for three parameters (L*a*b*) measured by colorimetry and photography from the results of three statistical analyses.
Color measurements obtained by digital photography were equivalent to those obtained using colorimetry. Thus, digital photography is a reliable, cost-effective measurement method of skin color and should be further investigated for quantitative analysis of surgical outcomes.
PMCID: PMC3072466  PMID: 19239578
Aesthetics; Breast Neoplasm; Clinical Photography; Reconstructive Surgical Procedures; Surgical Scars; Treatment Outcome
23.  Google Glass for Documentation of Medical Findings: Evaluation in Forensic Medicine 
Google Glass is a promising premarket device that includes an optical head-mounted display. Several proof of concept reports exist, but there is little scientific evidence regarding its use in a medical setting.
The objective of this study was to empirically determine the feasibility of deploying Glass in a forensics setting.
Glass was used in combination with a self-developed app that allowed for hands-free operation during autopsy and postmortem examinations of 4 decedents performed by 2 physicians. A digital single-lens reflex (DSLR) camera was used for image comparison. In addition, 6 forensic examiners (3 male, 3 female; age range 23-48 years, age mean 32.8 years, SD 9.6; mean work experience 6.2 years, SD 8.5) were asked to evaluate 159 images for image quality on a 5-point Likert scale, specifically color discrimination, brightness, sharpness, and their satisfaction with the acquired region of interest. Statistical evaluations were performed to determine how Glass compares with conventionally acquired digital images.
All images received good (median 4) and very good ratings (median 5) for all 4 categories. Autopsy images taken by Glass (n=32) received significantly lower ratings than those acquired by DSLR camera (n=17) (region of interest: z=–5.154, P<.001; sharpness: z=–7.898, P<.001; color: z=–4.407, P<.001, brightness: z=–3.187, P=.001). For 110 images of postmortem examinations (Glass: n=54, DSLR camera: n=56), ratings for region of interest (z=–8.390, P<.001) and brightness (z=–540, P=.007) were significantly lower. For interrater reliability, intraclass correlation (ICC) values were good for autopsy (ICC=.723, 95% CI .667-.771, P<.001) and postmortem examination (ICC=.758, 95% CI .727-.787, P<.001). Postmortem examinations performed using Glass took 42.6 seconds longer than those done with the DSLR camera (z=–2.100, P=.04 using Wilcoxon signed rank test). The battery charge of Glass quickly decreased; an average 5.5% (SD 1.85) of its battery capacity was spent per postmortem examination (0.81% per minute or 0.79% per picture).
Glass was efficient for acquiring images for documentation in forensic medicine, but the image quality was inferior compared to a DSLR camera. Images taken with Glass received significantly lower ratings for all 4 categories in an autopsy setting and for region of interest and brightness in postmortem examination. The effort necessary for achieving the objectives was higher when using the device compared to the DSLR camera thus extending the postmortem examination duration. Its relative high power consumption and low battery capacity is also a disadvantage. At the current stage of development, Glass may be an adequate tool for education. For deployment in clinical care, issues such as hygiene, data protection, and privacy need to be addressed and are currently limiting chances for professional use.
PMCID: PMC3936278  PMID: 24521935
Google Glass; forensic medicine; autopsy, postmortem examination; documentation
24.  Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques 
Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a male's ability to assess that female's reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a female's pre-fertile, ovulating, or post-fertile period. We printed colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receiver's ability to use a social partner's signals to discern their reproductive status.
PMCID: PMC3177625  PMID: 21471112
familiarity; experience; cognition; reproductive signals; ovulation; discrimination
25.  Brightness and Darkness as Perceptual Dimensions 
PLoS Computational Biology  2007;3(10):e179.
A common-sense assumption concerning visual perception states that brightness and darkness cannot coexist at a given spatial location. One corollary of this assumption is that achromatic colors, or perceived grey shades, are contained in a one-dimensional (1-D) space varying from bright to dark. The results of many previous psychophysical studies suggest, by contrast, that achromatic colors are represented as points in a color space composed of two or more perceptual dimensions. The nature of these perceptual dimensions, however, presently remains unclear. Here we provide direct evidence that brightness and darkness form the dimensions of a two-dimensional (2-D) achromatic color space. This color space may play a role in the representation of object surfaces viewed against natural backgrounds, which simultaneously induce both brightness and darkness signals. Our 2-D model generalizes to the chromatic dimensions of color perception, indicating that redness and greenness (blueness and yellowness) also form perceptual dimensions. Collectively, these findings suggest that human color space is composed of six dimensions, rather than the conventional three.
Author Summary
Vision scientists have long adhered to the classic opponent-coding theory of vision, which states that bright–dark, red–green, and blue–yellow form mutually exclusive color pairs. According to this theory, it is not possible to see both brightness and darkness at a single spatial location, or an extended set of locations, such as a uniform surface. One corollary of this statement is that all perceivable grey shades vary along a continuum from bright to dark. At first glance, the notion that brightness and darkness cannot coexist on a single surface accords with our common-sense notion that a given grey shade cannot be simultaneously both brighter and darker than any other grey shade. The results presented here suggest that this common-sense notion is not supported by experimental data. Our results imply that a given grey shade can indeed be simultaneously brighter and darker than another grey shade. This seemingly paradoxical conclusion arises naturally if one assumes that brightness and darkness constitute the dimensions of a two-dimensional perceptual space in which points represent grey shades. Our results may encourage scientists working in related fields to question the assumption that perceptual variables, rather than sensory variables, are encoded in opponent pairs.
PMCID: PMC2041963  PMID: 18237226

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