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Toothed whales use sound to find their way around, detect objects, and catch fish. They can investigate their environment by making clicking sounds, and then decoding the "echoic return signal" created when the clicking sounds bounce off objects and return to their ears. This "biosonar," called echolocation, is rare in the animal kingdom.

Now, a new study by researchers at the Woods Hole Oceanographic Institution, New College of Florida, UC Berkeley, and Oxford University, and in PLOS One, brings us closer to understanding how dolphin brains have evolved to support echolocation.

The research team applied new techniques for mapping networks in the excised brains of dead, stranded cetaceans to examine and compare the auditory pathways in echolocating dolphins and a non-echolocating baleen whale called a sei whale. A partnership with the International Fund for Animal Welfare (IFAW) and others is critical to advancing this work.

Baleen whales don't have teeth, but they and dolphins share a common ancestor, and both rely on complex vocal communication in a dark underwater environment. While dolphins have evolved echolocation, baleen whales have not. This newly published data is the first comparison of brain networks in dolphins and baleen whales and opens a new understanding of how brains have evolved to support active echolocation. The findings suggest that dolphin echolocation is more like "touching" with sound than "seeing" with sound.

According to Sophie Flem, a lead author and student in the inaugural class of New College of Florida's Marine Mammal Master's program, "Our research sought to understand how the pathways for auditory information differed between echolocating and non-echolocating whales. In humans, primates, rodents, and dogs, we have well-established maps of what parts of the brain contribute to what kind of processing. We don't yet have those in dolphin brains, which are strikingly unusual compared to terrestrial animal brains."

To work around this problem, the researchers tracked the pathways leaving a part of the midbrain called the inferior colliculus. This bilateral structure (one on the left, and one on the right) is shared across species and serves as a waystation for auditory information entering from the ear and going higher in the brain. Further, in dolphins, it's been previously studied and shown to be much larger relative to total brain size than in most terrestrial species. By taking advantage of this neural "chokepoint," the authors were able to confidently follow the path of auditory information in the dolphin brain, even into the largely uncharted cerebral cortex.

The results were surprising. Given that both dolphins and baleen whales rely on sensitive hearing for communication, but only dolphins echolocate, one might have expected the dolphins to have much stronger auditory projections. The echolocation clicks are so high in frequency that humans cannot hear them and produce a large amount of auditory information to process.

However, while the dolphins showed more projection sites in the cortex than the sei whale, the dolphin cortical projections were not stronger. Where the dolphins showed much stronger connections than the sei whale was in descending pathways going down from the inferior colliculi to the cerebellum. This offers a tantalizing clue about how dolphins echolocate.

"While neuroscientists used to think of the cerebellum largely as a center for balance and motor (muscle/movement) control, newer evidence strongly suggests that it serves as an integration center for sensory and motor information, and, importantly, a rapid prediction center," said Peter Tyack, Emeritus research scholar in Biology at WHOI, and a co-author on the study.

To explore their world through echolocation, animals must point their head in a direction of interest and make a narrow-beam echolocation click. "Think about groping for a light switch in a dark room, or using touch to figure out what object is inside a dark bag," said Tyack.

"Dolphins use echolocation to interact with their world, and, unlike hearing and vision, they must produce the energy that then returns to their sensory receptors—echolocation is part hearing and part vocalization. Think about moving your hand to produce the touch sense feedback that lets you find the light switch, similarly, dolphins move around their echolocation beam to get the feedback they need to function in a dark, underwater environment."

The stronger projections from the inferior colliculi to the cerebellum may help echolocators integrate auditory information with planning the production and direction of echolocation clicks to explore their environment.

Getting these brains imaged was a technical hurdle in itself. Although diffusion brain imaging has long been known to work on dead brains, it produces noisy, lower-quality images. Size is also a major factor—the giant sei whale brain used in this study was almost three times as big as a human brain, creating a number of complications.

These technical hurdles were solved by Karla Miller, at Oxford, who, over the last 10 years, has developed and refined new imaging sequences that greatly increase signal-to-noise ratio in brain diffusion imaging, and Ben Inglis, at UC Berkeley, who relentlessly optimized the data collection protocols.

The results are stunning, says senior author Peter Cook, an associate professor of Marine Mammal Science at New College of Florida, "Comparative neurobiologists have longed to examine the patterns of connections within dolphin and whale brains for years, believing that the unique evolutionary history of these species will provide new insights into how brains evolve. The technology is finally there to start to crack open these mysterious nervous systems and find out how they tick."

Having studied pathways for hearing in these species, the team is adding more brains, including new baleen brains, and next hopes to examine pathways related to vocal production. According to Cook, "It's believed that neural control of vocal output has totally shifted in dolphins as they evolved their unique nasal vocal apparatus. We can now map out vocal control in dolphins and how it differs from baleen whales.

"Both groups of animals have the rare ability to learn new vocal behavior, and dolphin vocal systems are some of the strangest in the animal kingdom. Now that we can opportunistically and ethically look inside these animals' brains, they're just getting started teaching us."