Wise Young Owls Help Unravel Behavior Development Puzzles

Eric Knudsen, Ph.D., knows why experience matters in the developing brain. A little bird told him.

Well, maybe it was a not-so-little bird with sharp claws that hunts mice at night.

Knudsen, the Edward C. and Amy H. Sewall Professor of Neurobiology at Stanford University School of Medicine, studies barn owls, and the birds are providing insights that may help psychiatrists understand the science connecting experience with behavior.

He discussed his work at the American Academy of Child and Adolescent Psychiatry's annual meeting in Honolulu last October. A second speaker talked about related effects in primates.

“Usually, we think of behavior as a physical manifestation, but we can also think of it as the information processing in underlying neural circuits,” said Knudsen.

Neural circuits are groups of connected neurons that function in both time and space. The regions where the circuits lie in the brain determine their function. However, specific sensitive periods in behavioral development affect the strength of the connections, as Knudsen found with the help of a flock of barn owls.

These windows for development explain why learning a second language is easier for children than adults, he said.

Knudsen has explored the owl's use of sound and vision to locate its prey to understand both where and when the birds develop behavioral abilities.

Like humans, owls use the time difference (just a few milliseconds) it takes for a mouse's squeak to arrive at each ear to locate the mouse in a horizontal plane. Owls also have feather flaps over each ear that help them differentiate sounds vertically.

Learning by Manipulating Sound

“So we can manipulate how sound gets to the owl's ear by putting a small device in its ear to shift its auditory aim point 55 milliseconds to one side,” explained Knudsen. “If the owl is young, it can make the neural adjustments and learn and recover its locating ability.”

He also placed Fresnel lenses in front of an owl's eyes to displace its visual field to one side to create a mismatch between the bird's visual and auditory fields.

After these optical changes, the owl at first could not locate its prey, but within six weeks, it had shifted its auditory aim point correctly to its target.

The owl's brain made that correction by rejecting inputs from the neurons it used before it was fitted with earmuffs or glasses and accepting signals from a newly developed circuit of neurons.

“New anatomical circuits form in the owl's brain,” said Knudsen. “The old circuit persists, but a new topographic map of auditory and visual space appears.”

When the experimental hardware is removed, the owl's brain goes back to using its former neural architecture in less time than it took to develop its new one.

But the capacity to learn doesn't last forever, he said. “Juveniles can shift the map fully, but at sexual maturity, around 7 months, they start losing that ability.”

All is not lost, however, and that is the lesson for psychiatrists. Experience lays down the neural tracks for future behavior.

“The juvenile experience has left its mark in the owl's brain,” said Knudsen. “The learned architecture persists into adulthood. Even as other connections are pruned away, these stick because they are useful as adaptive behavior.”

Attachment Forms in Primates

The mental life of owls may seem remote from human experience, so perhaps primates like macaque monkeys have more to teach us.

Baby macaques develop differently depending on the time when they are experimentally separated from their mothers, said Judy Cameron, Ph.D., a professor of psychiatry at the University of Pittsburgh, senior scientist at the Oregon National Primate Research Center, and a professor of behavioral neuroscience and obstetrics and gynecology at Oregon Health and Sciences University in Portland.

Cameron and colleagues placed mother-baby pairs of monkeys in a new social group a week after the baby's birth. Then at ages 1 week, 1 month, 3 months, and 6 months, they removed the mother from the cage. The youngest baby monkeys were bottle-fed until they could feed themselves.

The researchers looked at various outcomes, starting with ventral contact. Baby monkeys spend about 90 percent of their time in belly-to-belly contact with their mothers. In babies separated at 3 months of age, other mothers picked up the slack, and by 6 months of age there were no behavioral differences compared with controls. However, babies separated at 1 month rejected social overtures by other monkeys in the group at first.

“We equate this with a period of despair,” said Cameron. “But then they start to seek social contact and get up to 50 percent of their time in ventral contact.”

Babies separated at age 1 week showed no period of despair, however. They simply played alone, uninterested in social interaction, even when other monkeys tried to connect with them.

Other tests showed similar patterns, she said. When a mechanical car rolled into the playroom, most monkeys sought comfort with other animals. The ones separated at age 1 week clung to a snuggly toy, still demonstrating an aversion to social interaction. Also, when a human intruded into the monkeys' space and stared at the animals (which the monkeys normally consider a threat), the monkeys separated at 1 week of age looked once at the person then never looked their way again.

“They also did something else no other monkeys did,” said Cameron. “They exhibited stereotypy—thumbsucking or rocking back and forth, trying to comfort themselves.”

She tried an intervention as well, placing a baby for adoption by a willing, experienced mother monkey.

“These highly attentive mothers were able to remediate social behavior in the infants, but only if they were placed in the social group in the first month of life,” said Cameron. “If the placement with the highly attentive mother did not occur before 40 days, it was less effective than when it occurred at 1 month, and if it occurred at 3 months, it was not effective in normalizing the infants' social behavior. These babies had no interest in close social interaction.”

Other research by Cameron and her colleagues showed differential expression of the GUCY1A3 gene in the amygdala of monkeys separated at 1 week compared with those separated later or fully reared by their mothers.

All of this indicates that timing of early social bond disruption is critical, she said.

“Early life stress changes behavior, brain anatomy, and gene expression, but intervention works if it happens early enough,” she said.