Cortical determinants of human auditory cognition
Lead Research Organisation:
Newcastle University
Department Name: Biosciences Institute
Abstract
Hearing loss due to ear damage eventually affects half the population, is a major obstacle to work and home life, and a drain on the UK economy. If you ask anyone with common hearing loss what is wrong, they will NOT say 'I have lost 40 decibels at 2 kilohertz': the hearing-test result. They WILL say that they cannot hear colleagues at work in the canteen, or their family at dinner. Listening to speech in noise is much more complicated than the simple detection of sounds measured with hearing tests. We have to separate overlapping speech sounds and background noise that are louder than the sounds in hearing tests, group together speech elements into words and sentences, and associate those with meaning, which depends on our language exposure and ability. It is not surprising, then, that the hearing test, measuring the detection of tones in quiet, is not a good predictor of speech-in-noise ability, or the benefit from hearing devices. Two patients with the same hearing loss who are given the same hearing aids with the same improvement in their hearing tests can have strikingly different speech in noise ability after: so that one is happy with the result and the other throws the hearing aid away.
In this programme we will develop tests of the ability of subjects to group together and retain sounds that have a complex structure, like speech, and separate these from a noisy background. Unlike speech, the sounds are not associated with meaning, and their detection can be measured precisely in patients that speak different languages and have different language skills. These tests allow us to measure an important process that is more closely related to speech-in-noise analysis than simple hearing tests. The first tests we have used predict how well people hear speech in noise independently of simple hearing tests. We aim to develop further tests for the hearing clinic to predict how well people will manage in the real world: real world listening tests.
Although the tests we will develop assess what might be considered a simple process based on grouping and separation of sound elements, the analysis of these requires extensive processing in the brain, which we want to understand better. This analysis requires the auditory part of the brain, but also parts of the brain that are not usually considered parts of the auditory brain, including key structures usually associated with memory. Perhaps this is not surprising: sound stimuli, unlike static visual stimuli, evolve over time, and the separation of mixtures of sound requires us to remember or hold in mind the elements that form the foreground and background. In this work, we will measure brain activity that allows us to separate mixtures of sounds like speech in noise. We will use functional magnetic resonance imaging carried out on normal listeners when they carry out these tasks as an indirect measure of brain activity. We can also measure brain activity directly, in patients with epilepsy who have electrodes placed in the brain for a few days in order to work out where the epilepsy starts. As well as the localising their epilepsy, we can measure brain activity during listening tasks.
The outcome of these brain experiments will be the definition of brain systems for separating sounds like speech in noise. This will, firstly, provide other measures (in addition to the new listening tests) tests) of the success of interventions like hearing aids, cochlear implants, or hearing training. Secondly, the work will suggest possible interventions that might help patients to understand speech in noise. Although it may seem far fetched to try to improve speech-in-noise detection by interfering with the brain, there is already evidence that minimally invasive electrical stimulation can do this, and the work could identify brain targets for drug treatments.
In this programme we will develop tests of the ability of subjects to group together and retain sounds that have a complex structure, like speech, and separate these from a noisy background. Unlike speech, the sounds are not associated with meaning, and their detection can be measured precisely in patients that speak different languages and have different language skills. These tests allow us to measure an important process that is more closely related to speech-in-noise analysis than simple hearing tests. The first tests we have used predict how well people hear speech in noise independently of simple hearing tests. We aim to develop further tests for the hearing clinic to predict how well people will manage in the real world: real world listening tests.
Although the tests we will develop assess what might be considered a simple process based on grouping and separation of sound elements, the analysis of these requires extensive processing in the brain, which we want to understand better. This analysis requires the auditory part of the brain, but also parts of the brain that are not usually considered parts of the auditory brain, including key structures usually associated with memory. Perhaps this is not surprising: sound stimuli, unlike static visual stimuli, evolve over time, and the separation of mixtures of sound requires us to remember or hold in mind the elements that form the foreground and background. In this work, we will measure brain activity that allows us to separate mixtures of sounds like speech in noise. We will use functional magnetic resonance imaging carried out on normal listeners when they carry out these tasks as an indirect measure of brain activity. We can also measure brain activity directly, in patients with epilepsy who have electrodes placed in the brain for a few days in order to work out where the epilepsy starts. As well as the localising their epilepsy, we can measure brain activity during listening tasks.
The outcome of these brain experiments will be the definition of brain systems for separating sounds like speech in noise. This will, firstly, provide other measures (in addition to the new listening tests) tests) of the success of interventions like hearing aids, cochlear implants, or hearing training. Secondly, the work will suggest possible interventions that might help patients to understand speech in noise. Although it may seem far fetched to try to improve speech-in-noise detection by interfering with the brain, there is already evidence that minimally invasive electrical stimulation can do this, and the work could identify brain targets for drug treatments.
Technical Summary
Behavioural measures of pre-language auditory cognition will be developed that can account for the ability of subjects to hear speech in noise (SiN). This follows pilot work establishing that prototype non-speech auditory figure-ground (AFG) and auditory working memory (AFM) tests predict SiN independently of the audiogram. New tests will use stimuli that are closer to the spectrotemporal structure of speech.
fMRI at 3T will seek brain bases for the correlation between the non-speech behavioural measures and SiN. The work will test for common changes in BOLD activity in auditory regions as a function of task difficulty for AFG and SiN and for AWM and SiN. The work will also seek evidence for a common system for AFG and SiN and for AWM and SiN using modelling to identify common effects of the tasks on effective connectivity within and between auditory areas. fMRI at 3T on the AWM system will test the involvement of the hippocampus in AWM and in active tracking tasks. If the 3T experiments are successful, further work at 7T will allow more sensitive measurement of BOLD changes within subareas during the same tasks and more precise definition of time series to allow modelling of effective connectivity within and between auditory areas.
Neurophysiological recordings from neurosurgical patients will measure local field potentials (LFPs) to seek brain bases for the correlation between non-speech behavioural measures and SiN. Two groups of case studies with ten subjects each will be carried out to assess brain activity in auditory cortex during AFG and SiN tasks, and to assess activity in the network including auditory cortex, inferior frontal cortex and hippocampus during auditory working memory. Single unit recordings will be carried out from hippocampus and parahippocampus during AWM and auditory tracking tasks to seek human units that allow auditory computation.
fMRI at 3T will seek brain bases for the correlation between the non-speech behavioural measures and SiN. The work will test for common changes in BOLD activity in auditory regions as a function of task difficulty for AFG and SiN and for AWM and SiN. The work will also seek evidence for a common system for AFG and SiN and for AWM and SiN using modelling to identify common effects of the tasks on effective connectivity within and between auditory areas. fMRI at 3T on the AWM system will test the involvement of the hippocampus in AWM and in active tracking tasks. If the 3T experiments are successful, further work at 7T will allow more sensitive measurement of BOLD changes within subareas during the same tasks and more precise definition of time series to allow modelling of effective connectivity within and between auditory areas.
Neurophysiological recordings from neurosurgical patients will measure local field potentials (LFPs) to seek brain bases for the correlation between non-speech behavioural measures and SiN. Two groups of case studies with ten subjects each will be carried out to assess brain activity in auditory cortex during AFG and SiN tasks, and to assess activity in the network including auditory cortex, inferior frontal cortex and hippocampus during auditory working memory. Single unit recordings will be carried out from hippocampus and parahippocampus during AWM and auditory tracking tasks to seek human units that allow auditory computation.
Planned Impact
The work will benefit
- Those who develop clinically significant hearing loss during their lifetime (approximately half the population)
- Hearing professionals who assess them
- Policy makers
- Scientists and engineers interested in developing brain interventions to help real-life listening
- The UK economy
Mechanisms for benefit
- For patients, clinical tests developed during the lifetime of the project will better predict the benefit that patients might obtain from hearing restoration devices (especially common hearing aids), which will encourage their use in good prognosis, or suggest additional hearing rehabilitation otherwise
- Hearing professionals will be provided with objective measures to provide such prediction, to monitor responses, and to design rehabilitation strategies
- For policy makers, the measures will provide better data on the effects of hearing loss on the population using measures that can be applied to large numbers of people that are closer to real life listening than standard hearing tests, but easier to interpret than speech-based tests or questionnaires
- Also for policy makers, the work has the potential to explain how hearing loss, due to ear damage, contributes to degeneration in the brain, in dementia, strengthening further the public health argument for doing as much as possible to maintain hearing in middle age populations to prevent dementia
- For scientists and engineers, the work will identify brain targets for realistic interventions to help speech in noise like minimally invasive electrical stimulation
- The economy will benefit from measures to better predict and monitor the effects of hearing loss as a result of which more patients might actually use hearing restoration devices that are prescribed: hearing loss is estimated to cost the UK economy £30 billion per annum and a proportion of this is related to devices that are not used
Ways of maximising impact
- Public engagement to explain the research based on talks and website
- Making hearing professionals aware of new tests via clinical teaching and events carried out by group and via website
- Making scientists and engineers aware of brain study results via publications, scientific meetings and website
- Development of screening tools based on the tests developed that can be used in the community by smartphone
- Those who develop clinically significant hearing loss during their lifetime (approximately half the population)
- Hearing professionals who assess them
- Policy makers
- Scientists and engineers interested in developing brain interventions to help real-life listening
- The UK economy
Mechanisms for benefit
- For patients, clinical tests developed during the lifetime of the project will better predict the benefit that patients might obtain from hearing restoration devices (especially common hearing aids), which will encourage their use in good prognosis, or suggest additional hearing rehabilitation otherwise
- Hearing professionals will be provided with objective measures to provide such prediction, to monitor responses, and to design rehabilitation strategies
- For policy makers, the measures will provide better data on the effects of hearing loss on the population using measures that can be applied to large numbers of people that are closer to real life listening than standard hearing tests, but easier to interpret than speech-based tests or questionnaires
- Also for policy makers, the work has the potential to explain how hearing loss, due to ear damage, contributes to degeneration in the brain, in dementia, strengthening further the public health argument for doing as much as possible to maintain hearing in middle age populations to prevent dementia
- For scientists and engineers, the work will identify brain targets for realistic interventions to help speech in noise like minimally invasive electrical stimulation
- The economy will benefit from measures to better predict and monitor the effects of hearing loss as a result of which more patients might actually use hearing restoration devices that are prescribed: hearing loss is estimated to cost the UK economy £30 billion per annum and a proportion of this is related to devices that are not used
Ways of maximising impact
- Public engagement to explain the research based on talks and website
- Making hearing professionals aware of new tests via clinical teaching and events carried out by group and via website
- Making scientists and engineers aware of brain study results via publications, scientific meetings and website
- Development of screening tools based on the tests developed that can be used in the community by smartphone
Publications
Lad M
(2022)
A specific relationship between musical sophistication and auditory working memory.
in Scientific reports
Holmes E
(2021)
Active inference, selective attention, and the cocktail party problem.
in Neuroscience and biobehavioral reviews
Stefaniak JD
(2021)
Auditory beat perception is related to speech output fluency in post-stroke aphasia.
in Scientific reports
Holmes E
(2021)
Difficulties with Speech-in-Noise Perception Related to Fundamental Grouping Processes in Auditory Cortex
in Cerebral Cortex
Berger J
(2023)
Distribution of multiunit pitch responses recorded intracranially from human auditory cortex
in Cerebral Cortex
Dheerendra P
(2021)
Dynamics underlying auditory-object-boundary detection in primary auditory cortex.
in The European journal of neuroscience
Guo X
(2022)
EEG Responses to Auditory Figure-Ground Perception
Guo X
(2022)
EEG Responses to auditory figure-ground perception.
in Hearing research
Description | UKRI Future Leaders Fellowship Panel |
Geographic Reach | National |
Policy Influence Type | Influenced training of practitioners or researchers |
Impact | Selection of young researchers across the breadth of UKRI worthy of seven years of funding to establish careers in areas of innovation. |
Description | Auditory Cognition in Alzheimer's Disease |
Amount | £246,709 (GBP) |
Funding ID | MR/V006568/1 |
Organisation | Medical Research Council (MRC) |
Sector | Public |
Country | United Kingdom |
Start | 01/2021 |
End | 01/2024 |
Description | P50 |
Amount | $13,888,659 (USD) |
Funding ID | DC000242 |
Organisation | National Institutes of Health (NIH) |
Sector | Public |
Country | United States |
Start |
Description | Collaboration with Department of Otolayngology, University of Iowa Hospitals and Clinics, USA |
Organisation | University of Iowa |
Department | Department of Otolaryngology |
Country | United States |
Sector | Academic/University |
PI Contribution | I am PI running a project within a large NIH P50 grant to examine measures of sound analysis by the brain in subjects with cochlear implants. I employ staff at Iowa through this grant. The work is a direct extension of my work on normal auditory cognition subject as part of my WT and MRC programmes to patients with impaired hearing. |
Collaborator Contribution | Access to patients with cochlear implants who volunteer for research. |
Impact | PMID: 33387631; 32871106. |
Start Year | 2016 |
Description | Collaboration with Karl Friston |
Organisation | University College London |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Data from auditory imaging experiments |
Collaborator Contribution | Advice on analysis of imaging data and modelling |
Impact | List of PMIDs: 34687699; 27871729; 33136138; 24445167; 26787854; 21452943;17542641; 23055488; 17321704; 23716253 |
Description | Collaboration with Matthew Howard, Brain Research Laboratory, Department of Neurosurgery, University of Iowa Hospitals and Clinics, USA |
Organisation | University of Iowa |
Department | Department of Neurosurgery |
Country | United States |
Sector | Academic/University |
PI Contribution | 1. I carry out neurophysiological recordings from neurosurgical patients undergoing brain recordings before epilepsy surgery to examine bases for auditory cognition. This work is carried out with postdoctoral workers that I employ on WT programme grants to 2022 and MRC programme grant to 2025. The Director Howard is a Co-I on MRC programme grant. 2. I contribute to the core RO1 that supports the Iowa unit which pays 15% of my salary |
Collaborator Contribution | The Iowa neurosurgical team allows my team to have access to patients undergoing clinical recording and provides clinical care and appropriate IRB approval. |
Impact | PMIDs; 34246979; 33497775; 33482086; 33227284; 31401239; 29274745; 28441393; 28012852; 26949254; 25913402; 25632128; 24480831; 21452943; 20605456 |
Start Year | 2010 |
Description | Collaboration with neuropsychologist Eleanor Maguire |
Organisation | University College London |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | I run functional Imaging experiments at UCL in collaboration with Eleanor Maguire. I have a postdoctoral worker at UCL who carried these studies. |
Collaborator Contribution | Eleanor Maguire is Co-I on my MRC programme grant bases for auditory cognition. She provides intellectual input to work on the role of the hippocampus in auditory cognition and practical input to functional imaging experiments carried out at UCL. |
Impact | PMID 32871106 |
Start Year | 2019 |
Description | Collaboration with statistician Steven Rushton |
Organisation | Newcastle University |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | 1. Data collection of measures to explain relationship between auditory cognition in secondary-school children and language/literacy skill 2. Data collection of measures to explain relationship between auditory cognition and speech in noise. |
Collaborator Contribution | Partner is an expert in structural equation modelling of biological systems who advises on modelling of behavioural data. 1. He has contributed to modelling of a large school data set as part of the MRC project grant associated with this entry from 2019 2. He has contributed to planning of modelling of the behavioural data set as part of the MRC programme grant associated with this entry from grant submission |
Impact | 1. The school data are analysed and will form basis for report that is about to be submitted, which will be the main output of the MRC project grant 2. The behavioural data for the programme grants are not yet collected |
Start Year | 2019 |
Description | American Otological Society, Texas, 2022 (Presidential Lecture) |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Presidential Lecture to open the meeting of this organisation which is the second oldest medical society in North America that is a professional organisation comprising primarily otolaryngologist (ENT surgeons). My talk spoke to the need to consider brain mechanisms as well as ear mechanisms in patients with devices to restore peripheral hearing and that idea that hearing restoration might protect against dementia. |
Year(s) Of Engagement Activity | 2022 |
Description | Association for Research in Otolaryngology, USA, 2022 (invited speaker) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Invited talk at symposium on real-world listening in cochlear implant users. I presented data using measures developed on normal listeners in my WT and MRC programme grants that are now being applied to hearing impaired subjects. |
Year(s) Of Engagement Activity | 2022 |
Description | Auditory Processing Disorder Masterclass, UCL, 2020 and 2021 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Auditory Processing Disorder Workshop for clinical trainees in audiology. I taught on relevant auditory neuroscience related to my research programme in auditory cognitive neuroscience |
Year(s) Of Engagement Activity | 2020,2021 |
Description | Nottingham University Hearing Sciences Seminar Series, 2021 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Lecture on brain basis for link between hearing loss and dementia |
Year(s) Of Engagement Activity | 2021 |
Description | Plenary Speaker at Association fo British Neurologists Meeting 2022 |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Invited to give plenary lecture on auditory cognition at ABN meeting. Overview of work in programme grants and opportunity to establish further links to other dementia workers interested causal role of hearing loss |
Year(s) Of Engagement Activity | 2022 |
Description | Press coverage of work on emotional sound analysis |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Public/other audiences |
Results and Impact | Media coverage of work on a recently characterised disorder of emotional sound processing called misophonia in which we have suggested a new brain basis for the condition. 1. I did a radio interview on the BBC Radio 4 lunchtime news show that reached an audience of over 1M 2. I also did a more detailed piece on Radio 4 in 'The Curious Cases of Rutherford & Fry' 3. The work was covered by over 150 news outlets |
Year(s) Of Engagement Activity | 2021 |
URL | http://www.auditorycognition.org/media.html |
Description | Wisconsin University Hearing Seminar Series, 2021 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Talk on the basic science of auditory cognition |
Year(s) Of Engagement Activity | 2021 |