Special Features – Maney

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Exploring the Mind of Songbirds: Connecting gene sequence with the evolution of behavior

Kev Chapman

Perhaps the smartest bird that we know is the flamboyant Big Bird from Sesame

Street, who entertained our youths with a wide array of talents. He can roller skate, dance, draw, write poetry and even ride a unicycle. In reality, songbirds display complex cognitive and social behaviors. Therefore, they are excellent biological model for neurological research. Received her PhD in Neurobiology &

Behavior from the University of Washington in 1997 and has been at Emory since 2002, Dr. Donna Maney, the principle investigator of the Birdbrain Lab at the Emory Department of Psychology, is currently conducting research to evaluate the effects of hormones on brain structure and function in songbirds.

What was your concentration in graduate school? Why did you pick it?

Neurobiology and Behavior. I am interested in brain plasticity, in other words how the brain changes to respond to stimuli in adaptive ways.

Why songbirds?

Songbirds exhibit remarkable brain plasticity. Songbirds are famous for the large and obvious changes that occur in their brains in response to hormone fluctuations. You don’t even need a microscope to see differences in brain morphology between a bird with high vs. low testosterone, or between a male and a female. The magnitude of these changes, like the giant squid neurons, makes songbirds obvious models for studying plasticity, seasonality, and the neuroendocrine control of

behavior. They exhibit vocal learning. Songbirds and parrots are able to learn vocalization patterns from other members of their species, making their vocal development more similar to humans than any mammal. There is huge variation in social behavior across species. Researchers in the field of ornithology have been amassing an impressive body of literature pertaining to the social behavior of thousands of species of wild birds. As a result, we know for over 4,000 species whether they defend territories or live in social groups, whether they form pair bonds, how they communicate and how they care for their offspring. This database on behavior is unparalleled in any vertebrate group, and can be used to guide research into the neural mechanisms underlying pair bonding, aggression, sociality, parenting, and many other social behaviors. They are easily studied in their natural habitat. To be valuable and informative, research in neuroscience should be conducted using ethologically relevant tasks and contexts close the anima ls’ natural state. Few neuroscientists, however, are developing techniques to study wild populations. We are developing tools to study comparative behavioral neuroendocrinology in animals’ natural habitats. My research is not limited to songbirds. Over the course of my career, I have studied rats, mice, chickens, frogs, spiders and humans. Today, I am collaborating with other labs that work with humans, non-human primates, mice, and social insects.

Why conducting these studies?

Very little research, except possibly that conducted directly on humans, is aimed toward understanding the biology of only one type of organism.

Because the basic biology of every animal is the same, results obtained in one species are applicable on a broad level to others and to real life. Most biological research makes use of model organisms, or species that are well-suited for studying a particular question or system. For example,

Hodgkin and Huxley, scientists who studied how nerves conduct impulses, worked with squid because of their large neurons that were easy to study.

As a result, most of what we know about the conduction of nerve impulses in humans came from research on squid. Similarly, much of what we know about genes and pattern development in humans came from work on fruit flies. Songbirds are excellent models for our research questions.

What is the focus of your current research?

We have three projects that are ongoing. They focus on (1) the hormonal basis of sensory plasticity and how hormones alter motivation (2) how small changes in genetic sequence can have large effects on behaviors and (3) how seasonally breeding songbirds “know” it is time to breed each year.

What is the real life application of these projects?

The evolution of behavior relies on changes at the level of the genome; yet the ability to attribute a behavioral change to a specific, naturally occurring genetic change is rare in vertebrates. In white-throated sparrows, a genetic polymorphism segregates with a behavioral phenotype. Males and females of the white-striped (WS) morph are heterozygous for a rearranged chromosome 2, called ZAL2m, and respond to a simulated territorial intrusion with high levels of aggressive singing. Birds of the tan-striped (TS) morph are homozygous for the standard arrangement (ZAL2) and respond with relatively little or no singing. In addition to the difference in aggression, TS males engage in more parental behavior than WS males. Because of its association with aggressive and parental phenotypes, the ZAL2m chromosome represents a powerful target for studying the genes involved in these behaviors. We are using complementary approaches to identify genes that contribute to the behavioral phenotypes.

The Neurobiology of Social Reward: Conspecific vocalizations are special sounds. In some cases, animals will approach and even work to hear them; they have incentive salience . In female songbirds, the motivation to hear male song is dramatically altered by plasma levels of the reproductive hormone estradiol (E2). For example, female white-throated sparrows in non-breeding condition will press a key to hear male song several hundred times per day if they are treated with E2, whereas untreated females with low E2 are completely uninterested in hearing song. Our research goal is to understand exactly what E2 does in the brain to change the rewarding properties of social signals. A female whitecrowned sparrow responds to male song by performing a courtship display. Attending to a stimulus and assigning value to it both depend on monoamine neuromodulators such as dopamine and norepinephrine.

Neurons containing these catecholamines serve as dynamic filters that integrate ascending sensory signals with environmental context and internal state, allowing behavioral responses to change accordingly. We have shown that E2 alters these systems; for example, E2 increases the density of catecholaminergic and serotonergic fibers innervating auditory areas. We are now testing whether E2 modulates the sound-induced release of these monoamines in auditory and reward areas. Animal models are needed in order to understand autism and other human disorders of social reward. We are developing an assay to quantify social reward in zebra finches learning song. During the song learning period, juveniles are highly motivated to hear song and will peck a key to trigger song playback from a plastic model of an adult male. This assay nicely models social interactions between parent and offspring and will allow us to determine the effects of pharmacological manipulations on the reward value of those interactions. We are working closely with researchers at the

Marcus Autism Center in Atlanta to maximize the translational impact of our assay.

Environmental Modulation of Reproductive Function: Most living things use cues from the environment to time their reproductive efforts. For example, many seasonally breeding animals increase the secretion of reproductive hormones in response to lengthening days in the spring.

Other species use different kinds of cues, such as social context or food availability. How such signals are processed by the brain, and particularly how these signals are transduced into an endocrine response, is not well understood. Using a marker for new protein synthesis (Egr-1), we can map the brain’s response to cues in white-throated sparrows in the lab. By studying a model organism that responds to light cues with increases in hormone release, we can see that after just one long day, the mediobasal hypothalamus, a region at the base of the brain where reproductive hormones are released into the bloodstream, is actively producing Egr-1.

The Egr-1 indicates that this brain region is actively engaging in new gene transcription; in other words, responding to the environmental signal.

Since reproductive development can be accelerated in females when they hear male song, we played recordings of song to females in the lab in order to map the brain response. We found that within minutes, hearing song induces Egr-1 expression in the mediobasal hypothalamus and also triggers release of reproductive hormones. Our results suggest that cells in the mediobasal hypothalamus are part of a final common pathway for both kinds of environmental cue (light and sound). The research helps us to understand how the brain uses information from the external environment to bring about adaptive changes in the organism.

Are these projects different from what your lab has been doing for the past years?

Recent newer directions include operant conditioning tasks and RNA transcriptome analysis.

Would you give us a short description of the GA Tech lab that you are collaborating with?

Soojin Yi is the principle investigator at GA Tech. We were introduced by

Dr. James Thomas, formerly of Emory and now at NIH in Bethesda.

Why are you working with this lab?

Soojin is an expert in comparative genomics, which complements our expertise in behavioral neuroendocrinology. Together, we can ask questions about how genomic architecture can affect behavior and how behaviors evolve.

Why is it important for different universities/ organizations to collaborate in research?

You can’t always find exactly the right complementary expertise at your own institution, so it’s important to branch out.

Any advice for students who are interested in doing research in the future?

PIs are always interested in hearing from undergraduates who are interested in their research. The best way to contact a PI is by email. Be sure to use professional English (e.g. not “hey prof!”) and explain why you are interested in that PI’s research. I get a lot of emails from students who don’t bother to tell me why they want to work in my lab, and it’s obvious that they sent the email to a lot of different professors. Sometimes my name is in a different font or not mentioned at all. Emails like that are very unlikely to get a response. Take the time to explain yourself and show that you have a genuine interest in the research, because the PIs are looking for people who will get excited about the project.

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