Brain regions involved in speaking contribute to conscious awareness of speech

Matt Davis, MRC Cognition and Brain Sciences Unit, Cambridge, UK

Scientists in Cambridge have used brain imaging to show that conscious awareness of speech that is heard is associated with activity in regions of the brain that are involved in producing speech.

This result comes from collaborative research conducted in Cambridge by the Medical Research Council Cognition and Brain Sciences Unit (MRC CBSU) with assistance from the Impaired Consciousness Research Group, and the Division of Anaesthesia at the University of Cambridge. Dr Matt Davis and his colleagues used functional magnetic resonance imaging (fMRI) to map speech-related brain activity in volunteers at varying levels of awareness. Low doses of an anaesthetic drug were used to sedate the volunteers. The scientists measured how the brain’s response to speech changed as people became more sedated. The 12 volunteers, all anaesthetists, were scanned before and during sedation with propofol, a medicine commonly used to anaesthetise patients for surgery. Responses to sentences and to non-speech noises were assessed at three levels of awareness: fully awake, lightly sedated and heavily sedated. The heavy state didn’t go as far as general anaesthesia and all volunteers showed some response to the sound of speech, for instance, waking up when their name was called.

Dr. Davis, a cognitive neuroscientist at the MRC CBSU, and lead author on the paper, explained:

‘‘Everyone knows that if you have a conversation with someone as they are falling asleep they might not answer or have any memory of what you said. However, people who are soundly asleep might still wake up if their name is called. This observation suggests that some processing of speech remains possible even when people are unconscious. In this work, we asked: how does the brain’s response to speech change when people become unconscious?

Dr Davis and colleagues found that the more sedated the volunteers became, the less active their brains were in response to speech. Even at light levels of sedation, they saw no activity in brain areas that are normally used to comprehend sentences containing words with more than one meaning (ambiguous words like bark, or rain/reign). This suggested that despite being able to respond to simple questions, volunteers could no longer fully understand speech. Once more heavily sedated, brain areas involved in comprehending speech and storing sentences in memory became inactive.

One important finding was that brain regions involved in controlling the mouth, lips and tongue when speaking showed activity that was closely linked to the degree of conscious awareness of speech. Activity in the precentral gyrus an important part of the “motor system” of the brain was present when the volunteers were aware of hearing speech, but disappeared completely when they became unconscious and unresponsive. Dr Davis remarked:

To our surprise, the part of the brain in which showed the clearest change when people become unconscious was not an area involved in hearing speech sounds. Instead it was a region involved in producing speech that showed the most dramatic change in activity when our participants became so deeply sedated that they were no longer consciously aware of speech.

This finding is reminiscent of the “motor theory of speech perception” a controversial theory first proposed in the 1960s by Al Liberman of Yale University. Professor Liberman proposed that speech sounds can only be perceived using systems involved in speaking. In the intervening years, the motor theory was revised several times, but fell into disfavour in the 1980s since it was difficult to distinguish from theories in which our ability to make sense of speech sounds involves only those parts of the brain involved in hearing.

The motor theory is one of several accounts of speech perception that are an important focus of debate at the Acoustical Society meeting in Paris, France. A special session titled ‘Neurobiology of Speech Perception’ organized by Dr Paul Iverson (University College London) and Dr Christophe Pallier (INSERM CEA Cognitive Neuroimaging unit; Orsay, France) will present a range of evidence concerning the brain systems critical for hearing and understanding speech.

Dr Davis remarked:

“Several recent brain imaging studies have shown that the motor system lights up when people listen to speech, even if they are only have to lie still and listen. Our study provides evidence that motor activity is closely tied to conscious awareness of speech sounds - the inner voice that you hear in your head when listening to speech. The challenge now is to understand why the motor system responds when people hear speech. What is the function of activity in this region?

 Dr Davis and his colleagues at the Medical Research Council in Cambridge are currently conducting follow-up studies to answer this question. They are using brain imaging to measure motor activity in listening situations that make paying attention to the sounds of speech more important. For instance, when speech is heard through background noise or distortion, or when speech sounds are not clearly spoken people have to work hard to make sense of the speech that they hear.

In the meantime, however, this brain imaging method has implications for the care of patients undergoing general anaesthesia or emerging from a coma into a vegetative state. David Menon, British Oxygen Professor and Professor of Anaesthesia at the University of Cambridge, pointed out parallels in two clinical situations:

“First, a small proportion of anaesthetised patients report memories of events that occurred in the operating theatre, implying an inadvertent return of consciousness. Our research will help develop techniques to measure how deep anaesthesia needs to be to prevent awareness.”

 “Secondly, there is an emerging consensus that some severely brain-injured patients in a coma or vegetative state might understand but not be able to respond to speech. We can now use fMRI to detect to detect brain responses that are consistent with conscious awareness of speech”

Notes to editors

The finding comes from collaborative research conducted in Cambridge by the Medical Research Council Cognition and Brain Sciences Unit (MRC CBSU), the Impaired Consciousness Research Group, and the Division of Anaesthesia at the University of Cambridge. These studies were part of the research programme of the British Oxygen Professorship, funded by the Royal College of Anaesthetists. The full results are published in the Proceedings of the National Academy of Sciences. Researchers from University College London and Queen’s University, Ontario also contributed. The scanning took place at the Wolfson Brain Imaging Centre in Cambridge, UK.

Original research paper:

The following scientists collaborated on this research:

Matthew H, Davis and Adrian M. Owen of the MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK

• Martin R. Coleman and David K. Menon of the Impaired Consciousness Study Group, University of Cambridge, Cambridge, UK
• Anthony R. Absalom and Basil F. Matta of the Division of Anaesthesia, University of Cambridge, Addenbrookes Hospital, Cambridge, UK
• Jennifer M. Rodd of the Department of Psychology, University College London, London, UK
• Ingrid S. Johnsrude of the Department of Psychology, Queen's University, Kingston, Ontario, Canada

The Medical Research Council is dedicated to improving human health through excellent science. It invests on behalf of the UK taxpayer. Its work ranges from molecular level science to public health research, carried out in universities, hospitals and a network of its own units and institutes. The MRC liases with the Health Departments, the National Health Service and industry to take account of the public’s needs. The results have led to some of the most significant discoveries in medical science and benefited the health and wealth of millions of people in the UK and around the world. www.mrc.ac.uk