Vestigial auriculomotor activity indicates the direction of auditory attention in humans

Elife. 2020 Jul 3:9:e54536. doi: 10.7554/eLife.54536.

Abstract

Unlike dogs and cats, people do not point their ears as they focus attention on novel, salient, or task-relevant stimuli. Our species may nevertheless have retained a vestigial pinna-orienting system that has persisted as a 'neural fossil' within in the brain for about 25 million years. Consistent with this hypothesis, we demonstrate that the direction of auditory attention is reflected in sustained electrical activity of muscles within the vestigial auriculomotor system. Surface electromyograms (EMGs) were taken from muscles that either move the pinna or alter its shape. To assess reflexive, stimulus-driven attention we presented novel sounds from speakers at four different lateral locations while the participants silently read a boring text in front of them. To test voluntary, goal-directed attention we instructed participants to listen to a short story coming from one of these speakers, while ignoring a competing story from the corresponding speaker on the opposite side. In both experiments, EMG recordings showed larger activity at the ear on the side of the attended stimulus, but with slightly different patterns. Upward movement (perking) differed according to the lateral focus of attention only during voluntary orienting; rearward folding of the pinna's upper-lateral edge exhibited such differences only during reflexive orienting. The existence of a pinna-orienting system in humans, one that is experimentally accessible, offers opportunities for basic as well as applied science.

Keywords: auditory attention; electromyogram; human; neuroscience; pinna-orienting.

Plain language summary

Dogs, cats, monkeys and other animals perk their ears in the direction of sounds they are interested in. Humans and their closest ape relatives, however, appear to have lost this ability. Some humans are able to wiggle their ears, suggesting that some of the brain circuits and muscles that allow automatic ear movements towards sounds are still present. This may be a ‘vestigial feature’, an ability that is maintained even though it no longer serves its original purpose. Now, Strauss et al. show that vestigial movements of muscles around the ear indicate the direction of sounds a person is paying attention to. In the experiments, human volunteers tried to read a boring text while surprising sounds like a traffic jam, a baby crying, or footsteps played. During this exercise, Strauss et al. recorded the electrical activity in the muscles of their ears to see if they moved in response to the direction the sound came from. In a second set of experiments, the same electrical recordings were made as participants listened to a podcast while a second podcast was playing from a different direction. The individuals’ ears were also recorded using high resolution video. Both sets of experiments revealed tiny involuntary movements in muscles surrounding the ear closest to the direction of a sound the person is listening to. When the participants tried to listen to one podcast and tune out another, they also made ear ‘perking’ movements in the direction of their preferred podcast. The results suggest that movements of the vestigial muscles in the human ear indicate the direction of sounds a person is paying attention to. These tiny movements could be used to develop better hearing aids that sense the electrical activity in the ear muscles and amplify sounds the person is trying to focus on, while minimizing other sounds.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation
  • Adult
  • Aged
  • Attention*
  • Ear / physiology*
  • Electromyography
  • Humans
  • Middle Aged
  • Muscle, Skeletal / physiology*
  • Orientation / physiology*
  • Sound Localization / physiology*
  • Young Adult

Associated data

  • Dryad/10.5061/dryad.d4md86r