I was recently awarded an NIH National Research Service Award (NRSA) fellowship to pursue my postdoctoral research investigating the neural and genetic basis of aggression in Lake Malawi cichlid fish!
This work is on-going. Please stay tuned for updates!
Project Summary: The overarching goal of the proposed research is to investigate the neural and genetic basis of a naturally-occurring difference in aggressive behavior. Aggression has a strong genetic component, and yet we understand very little about how variation in the genome alters brain function to produce changes in behavior. Most of what is known about the relationship between genetic variants and social behavior comes from a small number of traditional lab model organisms. Using a novel natural vertebrate system, we employ an interdisciplinary approach to investigate the role of genetic polymorphisms in producing neural and behavioral variation. Rock- and sand-dwelling cichlid fishes from Lake Malawi in East Africa are closely-related and their genomes are very similar, yet they exhibit substantial diversity in social behaviors, including aggression. In Aim 1, I will quantify differences in aggressive behavior between rock- and sand-dwelling species and their hybrids. In Aim 2, I will first map the brain regions recruited during aggression by visualizing the expression of a marker of neural activity. Secondly, I will characterize the gene expression patterns of aggression-activated neurons by sequencing their transcriptomes, allowing us to discover novel genetic variants associated with differences in behavior. By comparing these results across species and their hybrids, we will provide insight into the neural and genomic mechanisms underlying phenotypic variation in aggression. In Aim 3, we will causally test the effect on brain and behavior of a candidate genetic variant in a vasopressin hormone receptor gene via CRISPR-Cas9 genome editing technology. This integrative approach is designed to provide insight into how variation in aggression can be produced by small changes to the sequence or regulation of genes. Taken together, this strategy will identify how the neural circuits regulating an essential social behavior are controlled at the level of the genome in outbred vertebrates, providing a model of behavioral diversity in humans.
Nicole M. Baran
Frontiers in Endocrinology
Research Topic: The Vasopressin System and Behavior
Vol. 8, No. 189 (August 2017)
Abstract: Nonapeptides, by modulating the activity of neural circuits in specific social contexts, provide an important mechanism underlying the evolution of diverse behavioral phenotypes across vertebrate taxa. Vasotocin-family nonapeptides, in particular, have been found to be involved in behavioral plasticity and diversity in social behavior, including seasonal variation, sexual dimorphism, and species differences. Although nonapeptides have been the focus of a great deal of research over the last several decades, the vast majority of this work has focused on adults. However, behavioral diversity may also be explained by the ways in which these peptides shape neural circuits and influence social processes during development. In this review, I synthesize comparative work on vasotocin-family peptides during development and classic work on early forms of social learning in developmental psychobiology. I also summarize recent work demonstrating that early life manipulations of the nonapeptide system alter attachment, affiliation, and vocal learning in zebra finches. I thus hypothesize that vasotocin-family peptides are involved in the evolution of social behaviors through their influence on learning during sensitive periods in social development.
Baran, N.M. (2017) Sensitive periods, vasotocin-family peptides, and the evolution and development of social behavior. Frontiers in Endocrinology. Research Topic: The Vasopressin System and Behavior. http://journal.frontiersin.org/article/10.3389/fendo.2017.00189/full
Nicole M. Baran, Samantha C. Peck, Tabitha H. Kim, Michael H. Goldstein, & Elizabeth Adkins-Regan
Proceedings of the Royal Society B: Biological Sciences
Vol. 284, No. 1859 (July 2017), pp. 20171114
Abstract: Vocal learning from social partners is crucial for the successful development of communication in a wide range of species. Social interactions organize attention and enhance motivation to learn species-typical behaviour. However, the neurobiological mechanisms connecting social motivation and vocal learning are unknown. Using zebra finches (Taeniopygia guttata), a ubiquitous model for vocal learning, we show that manipulations of nonapeptide hormones in the vasopressin family (arginine vasotocin, AVT) early in development can promote or disrupt both song and social motivation. Young male zebra finches, like human infants, are socially gregarious and require interactive feedback from adult tutors to learn mature vocal forms. To investigate the role of social motivational mechanisms in song learning, in two studies, we injected hatchling males with AVT or Manning compound (MC, a nonapeptide receptor antagonist) on days 2–8 post-hatching and recorded song at maturity. In both studies, MC males produced a worse match to tutor song than controls. In study 2, which experimentally controlled for tutor and genetic factors, AVT males also learned song significantly better compared with controls. Furthermore, song similarity correlated with several measures of social motivation throughout development. These findings provide the first evidence that nonapeptides are critical to the development of vocal learning.
Baran, N.M., Peck, S.C., Kim, T.H., Goldstein, M.H., Adkins-Regan, E. (2017) Early life manipulations of vasopressin-family peptides alter vocal learning. Proceedings of the Royal Society B: Biological Sciences. http://rspb.royalsocietypublishing.org/content/284/1859/20171114
Figure 1: GRN and SBN circuits. (A) Circuit diagram representing the GRN controlling forebrain specification at midlate gastrula stage. The diagram shows the regulatory activity of key developmental transcription factors implicated in the specification of the different forebrain domains. Modified from ref. 11. (B) Simplified circuit diagram representing the core social behavior neural network for aggression, plus several key regions in the mesolimbic reward pathway.
Nicole M. Baran, Patrick T. McGrath, & J. Todd Streelman
Proceedings of the National Academy of Science (PNAS)
Vol. 114, No. 23 (June 2017), pp. 5886–5893
Abstract: Animal behavior is ultimately the product of gene regulatory networks (GRNs) for brain development and neural networks for brain function. The GRN approach has advanced the fields of genomics and development, and we identify organizational similarities between networks of genes that build the brain and networks of neurons that encode brain function. In this perspective, we engage the analogy between developmental networks and neural networks, exploring the advantages of using GRN logic to study behavior. Applying the GRN approach to the brain and behavior provides a quantitative and manipulative framework for discovery. We illustrate features of this framework using the example of social behavior and the neural circuitry of aggression.
Baran, N.M., McGrath, P.T., Streelman, J.T. (2017) Applying gene regulatory network logic to the evolution of social behavior. Proceedings of the National Academy of Science. http://www.pnas.org/content/early/2017/05/30/1610621114
Early life manipulations of the nonapeptide system alter pair maintenance behaviors and neural activity in adult male zebra finches
Nicole M. Baran, Michelle L. Tomaszycki, & Elizabeth Adkins-Regan
Frontiers in Behavioral Neuroscience
Vol. 10, No. 58 (March 2016), pp. 1-10
Abstract: Adult zebra finches (T. guttata) form socially monogamous pair bonds characterized by proximity, vocal communication, and contact behaviors. In this experiment, we tested whether manipulations of the nonapeptide hormone arginine vasotocin (AVT, avian homolog of vasopressin) and the V1a receptor (V1aR) early in life altered species-typical pairing behavior in adult zebra finches of both sexes. Although there was no effect of treatment on the tendency to pair in either sex, males in different treatments exhibited profoundly different profiles of pair maintenance behavior. Following a brief separation, AVT-treated males were highly affiliative with their female partner but sang very little compared to Controls. In contrast, males treated with a V1aR antagonist sang significantly less than Controls, but did not differ in affiliation. These effects on behavior in males were also reflected in changes in the expression of V1aR and immediate early gene activity in three brain regions known to be involved in pairing behavior in birds: the medial amygdala, medial bed nucleus of the stria terminalis, and the lateral septum. AVT males had higher V1aR expression in the medial amygdala than both Control and antagonist-treated males and immediate early gene activity of V1aR neurons in the medial amygdala was positively correlated with affiliation. Antagonist treated males showed decreased activity in the medial amygdala. In addition, there was a negative correlation between the activity of V1aR cells in the medial bed nucleus of the stria terminalis and singing. Treatment also affected the expression of V1aR and activity in the lateral septum, but this was not correlated with any behaviors measured. These results provide evidence that AVT and V1aR play developmental roles in specific pair maintenance behaviors and the neural substrate underlying these behaviors in a bird.
Baran, N.M., Tomaszycki, M. L., Adkins-Regan, E. (2016) Early life manipulations of the nonapeptide system alter pair maintenance behaviors and neural activity in adult male zebra finches. Frontiers in Behavioral Neuroscience. http://journal.frontiersin.org/article/10.3389/fnbeh.2016.00058/full
Developmental effects of vasotocin and nonapeptide receptors on early social attachment and affiliative behavior in the zebra finch
Nicole M. Baran, Nathan C. Sklar, & Elizabeth Adkins Regan
Hormones and Behavior
Vol. 78 (February 2016), pp. 20-31
Abstract: Zebra finches demonstrate selective affiliation between juvenile offspring and parents, which, like affiliation between pair partners, is characterized by proximity, vocal communication and contact behaviors. This experiment tested the hypothesis that the nonapeptide arginine vasotocin (AVT, avian homologue of vasopressin) and nonapeptide receptors play a role prior to fledging in the development of affiliative behavior. Zebra finch hatchlings of both sexes received daily intracranial injections (post-hatch days 2–8) of either AVT, Manning Compound (MC, a potent V1a receptor antagonist) or saline (vehicle control). The social development of both sexes was assessed by measuring responsiveness to isolation from the family and subsequent reunion with the male parent after fledging. In addition, we assessed the changes in affiliation with the parents, unfamiliar males, and unfamiliar females each week throughout juvenile development. Compared to controls, MC subjects showed decreased attachment to the parents and MC males did not show the normal increase in affiliative interest in opposite sex individuals as they reached reproductive maturity. In contrast, AVT subjects showed a sustained affiliative interest in parents throughout development, and males showed increased interest in opposite sex conspecifics as they matured. These results provide the first evidence suggesting that AVT and nonapeptide receptors play organizational roles in social development in a bird.
Baran, N.M., Sklar, N.C., & Adkins-Regan, E. (2016) Developmental effects of vasotocin and nonapeptide receptors on early social attachment and affiliative behavior in the zebra finch. Hormones & Behavior. http://www.sciencedirect.com/science/article/pii/S0018506X15301021
Nicole M. Baran and Hudson Kern Reeve
The American Naturalist
Vol. 186, No. 5 (November 2015), pp. 594-609
Abstract: Here we develop a tug-of-war game theory model of mixed-strategy facultative parasitism. In this framework, individuals decide how to strategically invest in parental care effort, parasitism, and resistance to being parasitized, choosing their investments to respond optimally to their opponent’s behavior and vice versa. We have implemented the model in the well-studied case of mixed-strategy conspecific brood parasitism, which occurs when a female raises her own clutch of eggs and flexibly lays some eggs in a conspecific’s nest. However, the nest of a parasitic female in this case may also be parasitized. We model this as a tug-of-war, allowing parasitic and resistance efforts to strategically coevolve with each other. We then derive expressions for parasitism outcomes commonly observed in the field. The model also captures the trade-offs between parental care and parasitism when both are possible. We make a number of novel predictions about the rate of successful versus attempted parasitism as well as how parental care effort, resistance to parasitism, and fitness vary as functions of group size and individual differences between players in energy budget and production efficiency. Although we focus primarily on conspecific brood parasitism, the model is general enough to be extended to other systems in which facultative parasitism is possible, including the parasitism of food, fertilizations, nest sites, or other resources from conspecifics.
Baran, N.M. & Reeve, H.K. (2015). Co-evolution of parental care, parasitic, and resistance efforts in facultative parasitism. The American Naturalist. http://www.jstor.org/stable/10.1086/683227
Breeding experience, alternative reproductive strategies and reproductive success in a captive colony of zebra finches
Nicole M. Baran and Elizabeth Adkins-Regan
Vol. 9, No. 2 (February 2014), e89808
Abstract: Birds exhibit a remarkable diversity of different reproductive strategies both between and within species. Species such as the zebra finch (Taeniopygia guttata) may evolve the flexible use of alternative reproductive strategies, as well as benefit from prior breeding experience, which allows them to adaptively respond to unpredictable environments. In birds, the flexible use of alternative reproductive strategies, such as extra-pair mating, has been reported to be associated with fast reproduction, high mortality and environmental variability. However, little is known about the role of previous breeding experience in the adaptive use of alternative reproductive strategies. Here we performed an in-depth study of reproductive outcomes in a population of domesticated zebra finches, testing the impact of prior breeding experience on the use of alternative reproductive strategies and reproductive success. We provide evidence that older females with prior breeding experience are quicker to initiate a clutch with a new partner and have increased success in chick rearing, even in a captive colony of zebra finches with minimal foraging demands. We also find evidence that the breeding experience of other females in the same social group influences reproductive investment by female zebra finches. Furthermore, we demonstrate that the use of alternative reproductive strategies in female zebra finches is associated with previous failed breeding attempts with the same pair partner. The results provide evidence that age and breeding experience play important roles in the flexible use of both facultative and adaptive reproductive strategies in female zebra finches.
Baran N.M. & Adkins-Regan E. (2014) Breeding experience, alternative reproductivestrategies and reproductive success in a captive colony of zebra finches (Taeniopygia guttata). PLoS ONE 9(2): e89808. http://dx.doi.org/10.1371/ journal.pone.0089808