The auditory representation of speech sounds in human motor cortex

Abstract

In humans, listening to speech evokes neural responses in the motor cortex. This has been controversially interpreted as evidence that speech sounds are processed as articulatory gestures. However, it is unclear what information is actually encoded by such neural activity. We used high-density direct human cortical recordings while participants spoke and listened to speech sounds. Motor cortex neural patterns during listening were substantially different than during articulation of the same sounds. During listening, we observed neural activity in the superior and inferior regions of ventral motor cortex. During speaking, responses were distributed throughout somatotopic representations of speech articulators in motor cortex. The structure of responses in motor cortex during listening was organized along acoustic features similar to auditory cortex, rather than along articulatory features as during speaking. Motor cortex does not contain articulatory representations of perceived actions in speech, but rather, represents auditory vocal information.

DOI: http://dx.doi.org/10.7554/eLife.12577.001

eLife digest

When we speak, we force air out of our lungs so that it passes over the vocal cords and causes them to vibrate. Movements of the jaw, lips and tongue can then shape the resulting sound wave into speech sounds. The brain’s outer layer, which is called the cortex, controls this process. More precisely, neighboring areas in the so-called motor cortex trigger the movements in a specific order to produce different sounds.

Brain imaging experiments have also shown that the motor cortex is active when we listen to speech, as well as when we produce it. One theory is that when we hear a sound, such as the consonant ‘b’, the sound activates the same areas of motor cortex as those involved in producing that sound. This could help us to recognize and understand the sounds we hear.

To test this theory, Cheung, Hamilton et al. studied how speech sounds activate the motor cortex by recording electrical signals directly from the brain’s surface in nine human volunteers who were undergoing a clinical evaluation for epilepsy surgery. This revealed that speaking activates many different areas of motor cortex. However, listening to the same sounds activates only a small subset of these areas. Contrary to what was thought, brain activity patterns in motor cortex during listening do not match those during speaking. Instead, they depend on the properties of the sounds. Thus, sounds that have similar acoustic properties but which require different movements to produce them, such as ‘b’ and ‘d’, activate the motor cortex in similar ways during listening, but not during speaking.

Further research is now needed to work out why the motor cortex behaves differently when we hear as opposed to when we speak. Previous work has suggested that the region increases its activity during listening when the sounds heard are unclear, for example because of background noise. One testable idea therefore is that the motor cortex helps to enhance the processing of degraded sounds.

DOI: http://dx.doi.org/10.7554/eLife.12577.002