When Male Fish Hum Females Swim In, Thanks To Hormones, Adaptable Hearing

Researchers from the University of Washington and Cornell University have duplicated a natural physiological change that occurs in the female plainfin midshipman fish (Porichthys notatus) during the breeding season. Working with non-reproductive females, the researchers boosted hormone levels that alter the fish's inner-ear hearing sensitivity for a short period so they can better hear the males' humming calls.

"This is the first time anyone has been able to hormonally induce a change in hearing sensitivity in a vertebrate," said Joseph Sisneros, a UW assistant psychology professor who studies the neural basis of behavior. He is the lead author of a paper being published in the July 16 edition of the journal Science.

Sisneros and a Cornell research team headed by Andrew Bass, found that a spike in levels of the hormones testosterone and estradiol (an estrogen) triggers changes in the females' inner ear so they are capable of detecting higher frequencies in the males' multi-harmonic humming. This process couples the transmission of sound by the males and reception by the females.

"We suspected that enhancing the sensitivity of the females' ear to the upper harmonics of the males' hums should improve detection of their vocalization," said Bass, who is a professor of neurobiology and behavior. "Upper harmonics propagate farther in shallow-water environments like those where midshipman males build nests and sing their love songs to attract females. But the females can't process this vital information and respond appropriately if they can't hear it. Steroid hormones appear to provide a key molecule that leads to shifts in the hearing sensitivity of females."

The midshipman fish live in deep water off the Pacific Coast of the United States three-quarters of the year. They move into shallow intertidal zones to reproduce. Males build nests under rocks and begin broadcasting their loud humming love calls to attract females.

The researchers collected non-reproductive females, removed their ovaries and replaced them with implants to induce hormonal levels in the fish that mimic the natural spike in testosterone and estradiol levels in reproductive females. A month later the hormone implants caused changes in the non-reproductive females' hearing sensitivity.

"The importance of this study is that the neural plasticity we've uncovered may affect all vertebrates," said Sisneros. "This fish relies heavily on its auditory system for reproduction and our work gives us insight into how this plasticity operates. The next step is to locate where this plasticity occurs. There are four possibilities, at the sensory hair cells in the ear, in the auditory nerve, in the brain or in all three at the same time."

The jump is a big one, but Sisneros said the research eventually might have human applications. For instance, he said, "previous experiments in other laboratories suggest that steroid hormones may also play a role in causing some of the reported changes in hearing sensitivity of human females at differing stages of the menstrual cycle. Also humans have a natural loss of hearing in relationship to age. The higher frequencies tend to drop out first along with a natural drop in testosterone and estrogen. So a question arises: are natural decreases in hormone levels related to this loss of high-frequency hearing?"

Co-authors of the paper were Paul Forlano, a Cornell graduate student, and David Deitcher, a Cornell associate professor of neurobiology and behavior. They also identified the estrogen receptor in the female inner ear where the enhancement begins.

"This was especially important since estrogen receptors are also present in the human inner ear but no one know why they might be there. Our study now suggests a possible function," said Deitcher.

The National Institutes of Health funded the research.