'Love hormone' guides young songbirds in choice of 'voice coach'

Zebra finches are highly social birds and will press a lever in order to hear a recording of another Zebra finch singing. (Photo by Carlos RodrĆ­guez-Saltos)
By Carol Clark:  Oxytocin, the so-called “love hormone,” plays a key role in the process of how a young zebra finch learns to sing by imitating its elders, suggests a new study by neuroscientists at Emory University. Scientific Reports published the findings, which add to the understanding of the neurochemistry of social learning. “We found that the oxytocin system is involved from an early age in male zebra finches learning song,” says Natalie Pilgeram, first author of the study and an Emory PhD candidate in psychology. “It’s basic science that may lead to insights into the process of vocal learning across the animal kingdom, including humans.” “Our results suggest that the neurochemistry of early social bonds, particularly during language learning, may be relevant in studies of autism,” adds Donna Maney, a professor of neuroscience in Emory’s Department of Psychology and senior author of the study. Young male zebra finches learn to sing by listening to an adult male tutor that they choose to pay close attention to, normally their biological father or a “foster” father who nurtures them. This social process holds some similarities for how children learn to speak, making the birds a laboratory model for the neural underpinnings of social vocal learning. In the current paper, the researchers show how oxytocin, a hormone essential to social bonding, influences young finches exposed only to the songs of unfamiliar males. In experiments, blocking the young birds’ oxytocin receptors while they listened to a male biased the birds against that male’s song. Instead they preferred to listen to and eventually learn the song of a male they heard when their oxytocin receptors were allowed to function normally. The paper builds on previous work by the Maney lab regarding the hormonal and genetic influences on social behavior. Her lab is working with researchers at the Marcus Autism Center in Atlanta to maximize any potential translational impact of its research findings. Finding their voice: Zebra finches are highly social birds. In the wild they nest together in large colonies. Only adult males sing, primarily to court females. From the time they hatch, the males begin listening for song, and memorizing particular songs, even before they can actually sing one. “Up until around day 50, they are making little cheeps and warbles, what we call ‘subsong,’” Pilgeram explains. “It’s similar to human infants who begin to babble at around six months without actually talking.” During this sensitive listening phase, a male zebra finch pays closest attention to the song of its father, even though it can hear other adult males nearby. In a laboratory environment, research shows that if a biological father is removed from a cage before a male hatches and then substituted with a “foster father” that they can interact with, the young male will prefer the song of the foster father over other males it can hear. The young males demonstrate this preference by pressing levers that allow them to hear playback of different songs. Learning from their environment: “The young birds have got to learn all that they can from their environment,” Pilgeram says. “Just as during human development, the birds pay the closest attention to their immediate caregivers, on whom they rely for everything.” Around day 50, the young male finches enter puberty and what is called the “plastic song phase.” During this time, they practice their song motor skills and actively try to produce song. Although they begin to shift their attention away from their fathers and show a preference for hearing songs of other males, each young male still practices dad’s tune. By day 100, most male zebra finches are fully singing their father’s song. They have reached adulthood and their tune has “crystalized” into the song that they will sing for the rest of their lives. In previous research, the Maney lab found that the stronger the preference a male zebra finch shows for its father’s song during the early listening phase, the more closely its crystalized adult song will mimic that of the father. The role of oxytocin: For the current paper, the researchers wanted to test whether the oxytocin system played a role in that preference. The research centered on male juvenile zebra finches hatched in the lab. At day four, the fathers were removed from each of the youngsters’ cages so they were raised only by their mothers. The cages were enclosed in chambers that prevented the young birds from hearing song from other birds housed nearby. Beginning at day 27 in a young bird’s life, it was exposed to a series of tutoring sessions by two different adult male tutors that it had never heard. The tutor’s cage was placed next to the cage of the young bird, or pupil. When it was exposed to one of the tutors, the pupil was given a substance that blocked its oxytocin receptors from activating. When the young bird was exposed to the other tutor it received a control substance that allowed its oxytocin receptors to function normally. After completing a series of tutoring sessions, the pupils were presented with two different levers they could press in their cages. Pressing one lever was more likely to play the song they heard when their oxytocin receptors were blocked. The other lever was more likely to play the song they heard with normally functioning oxytocin. The results showed that early in their development, the juveniles favored the song that they heard when their oxytocin was not blocked. Building on past findings: “We also found that when their oxytocin was not blocked, the birds’ developmental milestones fit the same data curve as in our previous research,” Maney says. “They showed an early preference for the song of one tutor, then switched to preferring the other song during puberty.” The preference flattened out as they began singing the song of their chosen tutor, she adds. And the stronger the preference that they showed for the chosen tutor’s song during the early listening phase, the more closely their own adult song resembled that of the chosen tutor. The researchers also noted behavioral differences in the way the pupils and tutors interacted. With normally functioning oxytocin, a pupil pecked more often at the wall of its cage facing the tutor and more often preened in a fashion known to be associated with focused listening in the birds, compared to when its oxytocin was blocked. “Our results suggest that the oxytocin system is involved in how an animal decides where to focus its attention very early in its life,” Pilgeram says. Co-authors of the study include Carlos RodrĆ­guez-Saltos, who received his doctorate from Emory and is now at Illinois State University; postdoctoral fellow Nicole Baran; research technicians Matthew Davis and Erik Iverson; and Emory undergraduates Sumin Lee, Emily Kim and Aditya Bhise. The work was funded by the National Science Foundation and the Silvio O. Conte Center for Oxytocin and Social Cognition. Source: eScienceCommons
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How grandmothers' brains react to the sight of their grandchildren

"We're highlighting the brain functions of grandmothers that may play an important role in our social lives and development," says Minwoo Lee, an Emory graduate student and co-author of the study. "It's an important aspect of the human experience that's been largely left out of the field of neuroscience."

By Carol Clark: Many people lucky enough to have grown up with doting grandmothers know that they can burnish a child’s development in unique and valuable ways. Now, for the first time, scientists have scanned grandmothers’ brains while they’re viewing photos of their young grandchildren — providing a neural snapshot of this special, inter-generational bond.

Proceedings of the Royal Society B published the first study to examine grandmaternal brain function, conducted by researchers at Emory University.

“What really jumps out in the data is the activation in areas of the brain associated with emotional empathy,” says James Rilling, lead author and professor in Emory's Department of Anthropology and Department of Psychiatry and Behavioral Sciences. “That suggests that grandmothers are geared toward feeling what their grandchildren are feeling when they interact with them. If their grandchild is smiling, they’re feeling the child’s joy. And if their grandchild is crying, they’re feeling the child’s pain and distress.”

In contrast, the study found that when grandmothers view images of their adult child, they show stronger activation in an area of the brain associated with cognitive empathy. That indicates they may be trying to cognitively understand what their adult child is thinking or feeling and why, but not as much from the emotional side.

“Young children have likely evolved traits to be able to manipulate not just the maternal brain, but the grand maternal brain,” Rilling says. “An adult child doesn’t have the same cute ‘factor,’ so they may not illicit the same emotional response.”

Co-authors of the study are Minwoo Lee, a PhD candidate in Emory’s Department of Anthropology, and Amber Gonzalez, a former Emory research specialist.
"What really jumps out in the data is the activation in areas of the brain associated with emotional empathy," Rilling says.

“I can relate to this research personally because I spent a lot of time interacting with both of my grandmothers,” Lee says. “I still remember warmly the moments I had with them. They were always so welcoming and happy to see me. As a child, I didn’t really understand why.”

It’s relatively rare, Lee adds, for scientists to study the older human brain outside of the problems of dementia or other aging disorders.

“Here, we’re highlighting the brain functions of grandmothers that may play an important role in our social lives and development,” Lee says. “It’s an important aspect of the human experience that has been largely left out of the field of neuroscience.”

Rilling’s lab focuses on the neural basis of human social cognition and behavior. Motherhood has been extensively studied by other neuroscientists. Rilling is a leader in researching the lesser-explored neuroscience of fatherhood.

Grandmothers interacting with grandchildren offered new neural territory.

“Evidence is emerging in neuroscience for a global, parental caregiving system in the brain,” Rilling says. “We wanted to see how grandmothers might fit into that pattern.”

Humans are cooperative breeders, meaning that mothers get help caring for their offspring, although the sources of that help vary both across and within societies.

“We often assume that fathers are the most important caregivers next to mothers, but that’s not always true,” Rilling says. “In some cases, grandmothers are the primary helper.”

In fact, the “grandmother hypothesis” posits that the reason human females tend to live long past their reproductive years is because they provide evolutionary benefits to their offspring and grandchildren. Evidence supporting this hypothesis includes a study of the traditional Hadza people of Tanzania, where foraging by grandmothers improves the nutritional status of their grandchildren. Another study of traditional communities showed that the presence of grandmothers decreases their daughters’ interbirth intervals and increases the number of grandchildren.

And in more modern societies, evidence is accumulating that positively engaged grandmothers are associated with children having better outcomes on a range of measures, including academic, social, behavior and physical health.
"If their grandchild is smiling, they're feeling the child's joy," Rilling says. "And if their grandchild is crying, they're feeling the child's pain and distress."

For the current study, the researchers wanted to understand the brains of healthy grandmothers and how that may relate to the benefits they provide to their families.

The 50 participants in the study completed questionnaires about their experiences as grandmothers, providing details such as how much time they spend with their grandchildren, the activities they do together and how much affection they feel for them. They also underwent functional magnetic resonance imaging (fMRI) to measure their brain function as they viewed pictures of their grandchild, an unknown child, the same-sex parent of the grandchild, and an unknown adult.

The results showed that, while viewing pictures of their grandchildren, most participants showed more activity in brain areas involved with emotional empathy and movement, compared to when they were viewing the other images.

Grandmothers who more strongly activated areas involved with cognitive empathy when viewing pictures of their grandchild reported in the questionnaire that they desired greater involvement in caring for the grandchild.

Finally, compared with results from earlier study by the Rilling lab of fathers viewing photos of their children, grandmothers more strongly activated regions involved with emotional empathy and motivation, on average, when viewing images of their grandchildren.

“Our results add to the evidence that there does seem to be a global parenting caregiving system in the brain, and that grandmothers’ responses to their grandchildren maps onto it,” Rilling says.

One limitation to the study, the researchers note, is that the participants skewed towards mentally and physically healthy women who are high-functioning grandmothers.

The study opens the door to many more questions to be explored. “It would be interesting to also look at the neuroscience of grandfathers and how the brain functions of grandparents may differ across cultures,” Lee says.

An especially gratifying aspect of the project for Rilling was personally interviewing all the participants himself. “It was fun,” he says. “I wanted to get a sense of the rewards and challenges of being a grandmother.”

The main challenge many of them reported was trying not to interfere when they disagreed with the parents over how their grandchildren should be raised and what values should be instilled in them.

“Many of them also said how nice it is to not be under as much time and financial pressure as they were when raising their children,” Rilling says. “They get to enjoy the experience of being a grandmother much more than they did being parents.” This work was supported in part by the Silvia O. Conte Center for Oxytocin and Social CognitionSource eScienceCommons:
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