How mice block out the sound of their own feet

A mouse’s brain has a built-in noise-cancelling circuit to ensure that the mouse hears the sounds of an approaching cat better than it hears the sounds of its own footsteps, according to new research.

It’s a direct connection from the motor cortex of the brain to the auditory cortex that says essentially, “we’re running now, pay no attention to the sound of my footsteps.”

“What’s special about this cancellation process is that the brain learns to turn off responses to predictable self-generated sounds,” says Richard Mooney, a professor of neurobiology at Duke University. “You can watch as these responses disappear as a function of time and experience.”

The findings, which appear in Nature, come from an array of difficult experiments, including a “mouse virtual reality” setup.

Cut the noise

This brain circuitry works differently than noise-cancelling headphones, but the results are similar. The headphones monitor ambient noise around the listener and then produce sounds that are mirror images of those soundwaves to cancel them out. Similarly, the brain’s auditory cortex receives a signal directly from the motor cortex that tells its inhibitory neurons to selectively cancel out the sounds it has learned will come from a particular motion.

For this system to work, it cannot depend solely on input from the ears, Mooney says, “because by the time the auditory signal from the ear is processed by the brain, it’s old news.”

In fact, the motor cortex sends the cancellation signal to the auditory cortex in parallel with commanding a movement, a process so fast that cancellation in the auditory cortex is actually predictive.

“The sound of the first footstep isn’t heard,” says David Schneider, a former Duke postdoctoral researcher in Mooney’s lab who is now an assistant professor at New York University’s Center for Neural Science.

“We would have a hard time operating in the natural world, if we couldn’t predict the sensory consequences of moving around in it,” says Mooney, who has also studied the connection between the auditory cortex and the motor cortex as birds learn to sing.

Digging deeper

To monitor the circuit, Schneider and graduate student Janani Sundararajan trained mice to associate an artificial tone with their foot-falls. As the mice walked or ran on a treadmill in this “virtual reality” experiment, the tone’s tempo matched each pitter-pat.

“We decided to make the sound as artificial as possible to push the mouse’s brain beyond what it was evolved to do,” Schneider says.

Schneider and Sundararajan watched the mouse’s brain as synapses that the motor cortex makes in the auditory cortex changed as it learned to cancel a predictable movement-related noise. They were able to identify the inhibitory neurons that responded to the artificial tone to cancel out its signal, “exactly like noise cancelling,” Schneider says.

To confirm what they were seeing, Sundararajan then did a series of behavioral experiments in which mice were taught to seek a reward after hearing two different tones. Then she trained them on the treadmill as before to associate one of those tones with walking.

After training, the mice detected the non-associated tone better than the “walking” tone when they were actually walking, even though they detected both tones equally well when they were standing still.

“The brain would rather be more sensitive to noises other than the ones we make,” Sundararajan says. For a mouse being stalked by a nearby cat, it would be a matter of survival.

What this means for humans

Being able to ignore the sounds of one’s own movements is likely important for humans as well. But the ability to anticipate the sounds of our actions is also important for more complex human behaviors such as speaking or playing music.

“When we learn to speak or to play music, we predict what sounds we’re going to hear—such as when we prepare to strike keys on a piano—and we compare this to what we actually hear,” explains Schneider. “We use mismatches between expectation and experience to change how we play—and we get better over time because our brain is trying to minimize these errors.”

Being unable to make predictions like this is also thought to be involved in a spectrum of afflictions.

“Overactive prediction circuits in the brain are thought to lead to the voice-like hallucinations associated with schizophrenia while an inability to learn the consequences of one’s actions could lead to debilitating social paralysis, as in autism,” explains Schneider.

“By figuring out how the brain normally makes predictions about self-generated sounds, we open the opportunity for understanding a fascinating ability—predicting the future—and for deepening our understanding of how the brain breaks during disease.”

The Howard Hughes Medical Institute, the Helen Hay Whitney Foundation, Burroughs Wellcome Fund, a Holland-Trice Graduate Fellowship in Brain Sciences, and the National Institutes of Health supported the research.

Source: Duke University, New York University