Elsevier

Brain and Language

Volume 222, November 2021, 105009
Brain and Language

Improving speech perception in noise in young and older adults using transcranial magnetic stimulation

https://doi.org/10.1016/j.bandl.2021.105009Get rights and content

Highlights

  • Speech perception declines with age independently of hearing acuity and cognition.

  • Age-related speech perception decline affects all types of phonemic contrasts.

  • iTBS to the left PMv and pSTS can enhance speech perception in adults of all ages.

  • iTBS to the left PMV is associated with greater improvement in performance.

  • Behavioral changes induced by iTBS are affected by baseline performance level.

Abstract

Normal aging is associated with speech perception in noise (SPiN) difficulties. The objective of this study was to determine if SPiN performance can be enhanced by intermittent theta-burst stimulation (iTBS) in young and older adults.

Method

We developed a sub-lexical SPiN test to evaluate the contribution of age, hearing, and cognition to SPiN performance in young and older adults. iTBS was applied to the left posterior superior temporal sulcus (pSTS) and the left ventral premotor cortex (PMv) to examine its impact on SPiN performance.

Results

Aging was associated with reduced SPiN accuracy. TMS-induced performance gain was greater after stimulation of the PMv compared to the pSTS. Participants with lower scores in the baseline condition improved the most.

Discussion

SPiN difficulties can be reduced by enhancing activity within the left speech-processing network in adults. This study paves the way for the development of TMS-based interventions to reduce SPiN difficulties in adults.

Introduction

Older adults often report difficulties following conversations in noisy environments (e.g., at the restaurant or during family reunions), which can hinder social interactions (Aydelott et al., 2010, O, 1988). Several studies have shown that peripheral hearing only partially explains these difficulties, which suggests a contribution of central mechanisms (e.g. Anderson et al., 2013, Dubno et al., 2008, Fostick et al., 2013, Humes and Dubno, 2010, Pichora-Fuller and Souza, 2003). One possibility is that speech perception in noise (SPiN) difficulties are triggered by age-related decline in brain regions supporting central auditory mechanisms in the primary auditory cortex (transverse temporal gyrus; TTG). Alternatively, these difficulties could be related to aging of the brain networks supporting speech functions. Indeed, in addition to involving the primary auditory cortex, processing speech also activates regions involved in phonological (e.g., the superior temporal cortex; STC), motor (e.g., the primary motor and premotor cortex; PM) and lexical (e.g., the middle temporal gyrus; MTG) processes, as well as regions of the executive network, such as the middle frontal cortex, cingulate cortex, frontal operculum and anterior insula (e.g. Adank, 2012, Alain et al., 2018, Eckert et al., 2016).

Consistent with the notion of a role for higher-order processes in age-related decline in SPiN, several brain imaging studies have shown that structural decline in brain areas and white matter tracts that support phonological (e.g., the bilateral STC), motor (e.g., the PM), lexical (e.g., the MTG), and attention-related processes (e.g., the insula) is associated with speech performance decline (e.g. Bilodeau-Mercure et al., 2015, Eckert et al., 2008, Sheppard et al., 2011, Tremblay et al., 2021, Wong et al., 2010). For instance, in a group of older adults, accuracy during a sentence repetition task was found to be predicted by cortical thickness of the left superior frontal gyrus and hemispheric volume of the left pars triangularis gyrus (Wong et al., 2010).

Differences in cerebral activation patterns between young and older adults have also been found during SPiN tasks within auditory, phonological and lexical processing areas (e.g. Du and Alain, 2016, Hwang et al., 2007, Manan et al., 2015, Manan et al., 2017, Tremblay et al., 2020, Wong et al., 2009), as well as sensorimotor (e.g. Bilodeau-Mercure et al., 2015, Du and Alain, 2016, Eckert et al., 2008, Manan et al., 2017, Peelle et al., 2010) and attention-related areas (e.g. Bilodeau-Mercure et al., 2015, Du and Alain, 2016, Eckert et al., 2008, Peelle et al., 2010; Vaden et al., 2015, Wong et al., 2009). For instance, a study from our group showed a detrimental indirect effect of age on syllable repetition errors (Bilodeau-Mercure et al., 2015). In that study, aging was associated with lower activation in the left anterior insula, which in turn was associated with decreased accuracy. In a recent study, it was found that when performance in a syllable identification task was matched between younger and older adults, older adults showed higher activity in areas including the bilateral STG, MTG, MFG and precentral gyrus, as well as the left ventral premotor cortex (PMv) and left IFG, suggesting that compensation within speech processing areas contributed to maintaining performance (Du & Alain, 2016). Another study found that the bilateral anterior cingulate cortex (ACC) and the left MFG were more engaged in older adults during degraded word recognition for correct compared to incorrect answers (Eckert et al., 2008). Together, brain imaging studies show that the network supporting SPiN declines with age, and that this decline is associated with a decline in performance. The question that we address here is whether SPiN performance can be enhanced using non-invasive brain stimulation methods.

Non-invasive brain stimulation methods, such as transcranial magnetic stimulation (TMS), can induce beneficial short and longer-term plasticity in the brain, which can lead to enhanced performance in a variety of domains, including motor performance (e.g. Hoyer and Celnik, 2011, Lüdemann-Podubecká et al., 2015, Schambra, 2018), cognition (e.g. Guse, Falkai, & Wobrock, 2010; Kim et al., 2019, Widhalm and Rose, 2019), hearing (e.g. Chen et al., 2020, Schoisswohl et al., 2019, Soleimani et al., 2016), and speech/language (e.g. Devlin and Watkins, 2007, Li et al., 2020). Intermittent theta-burst stimulation (iTBS), a repetitive TMS (rTMS) protocol that can increase cortical excitability, is a promising method to enhance performance during speech tasks in healthy adults and in those with communication disorders. Consistent with this notion, one study has shown that iTBS over the pIFG increased accuracy in sentence repetition in healthy young adults (Restle, Murakami, & Ziemann, 2012). Another study showed enhanced vocal pitch regulation in healthy young adults after iTBS over the right somatosensory laryngeal cortex, during a pitch-matching singing task with masked feedback (Finkel et al., 2019). Several studies of post-stroke aphasic patients have shown that language functions (e.g., semantic fluency, picture naming, auditory comprehension) can be improved by applying iTBS over the left IFG or left temporal cortex in young and older adults (Griffis et al., 2016, Szaflarski et al., 2018, Szaflarski et al., 2011, Versace et al., 2019, Vuksanović et al., 2015). Together, these studies suggest that the adult speech/language system is plastic, and that performance can be boosted using faciliatory rTMS such as iTBS.

To our knowledge, iTBS has never been used to induce changes in the speech network in healthy older adults. A limited number of studies have shown that iTBS applied to the motor cortex can successfully increase cortical excitability in healthy older adults (e.g. Dickins et al., 2015, Gedankien et al., 2017, Young-Bernier et al., 2014). Yet, a recent meta-analysis reported reduced motor evoked potential (MEP) amplitudes and longer latencies in older compared to younger individuals after single-pulse, paired pulse or rTMS was applied (Tang et al., 2019). Specifically, the analysis of 20 studies using electromyography to measure cortical excitability in the primary motor cortex showed that MEP responses to TMS had a significantly lower amplitude in elderly compared to younger adult groups, though the MEP responses were significant in both groups. Another analysis including seven studies showed that post TMS MEP latency was delayed in the elderly group compared to the younger group. Although MEP activity measures can be influenced by age-related factors other than brain plasticity itself (e.g., skin and skull characteristics), at least one study has shown that MEP amplitude changes after motor cortex iTBS correlate with TMS-evoked EEG potentials. This suggests that post-iTBS MEP changes are representative of brain activity changes (Gedankien et al., 2017). Together with findings from clinical populations, these findings suggest that TMS can induce neuroplasticity in the aging brain, though the potential for plasticity may be reduced in older compared to younger adults. Additional evidence is needed regarding the potential for plasticity within specific functional systems such as the speech/language system in the aging brain.

The main objectives of this two-part study were (1) to investigate the mechanisms underlying age-related SPiN decline, and (2) to determine if SPiN performance in young and older adults can be enhanced by excitatory rTMS to two areas involved in processing sublexical speech: the left posterior superior temporal sulcus or pSTS, and the left ventral premotor cortex or PMv. The selection of these areas was based on knowledge of their role in SPiN, and prior evidence that TMS to these regions can successfully induce behavioural changes in healthy young adults. The left pSTS is involved in sublexical phonological processing (e.g. Hickok and Poeppel, 2007, Turkeltaub and Coslett, 2010). For instance, a recent study has shown that inhibitory TMS to this region is associated with phonological errors during auditory word comprehension, syllable repetition, syllable identification and pseudo-word repetition (Murakami, Kell, Restle, Ugawa, & Ziemann, 2015). Another study found that rTMS applied to the anterior STS led to poorer performance during sentence repetition in noise (Kennedy-Higgins, Devlin, Nuttall, & Adank, 2020). The left PMv is involved in speech perception and comprehension (e.g. McGettigan and Tremblay, 2018, Pulvermuller and Fadiga, 2010, Tremblay and Small, 2011, Walenski et al., 2019). Although the specific contribution of this region is still unclear and a subject of debate, previous studies have shown that inhibitory rTMS to this region is associated with reduced speech perception performance (Krieger-Redwood, Gaskell, Lindsay, & Jefferies, 2013; I. G. Meister et al., 2007, Sato et al., 2009) or enhanced selective adaptation to speech during speech perception (Grabski, Tremblay, Gracco, Girin, & Sato, 2013).

The specific objectives of Experiment 1 were to develop and test an age-sensitive sub-lexical SPiN test and to examine the impact of cognition and hearing on performance at this test. Our main hypothesis was that aging would be associated with reduced SPiN performance operationalized as lower accuracy and longer reaction times (RT), after controlling for hearing and cognition. The specific objective of Experiment 2 was to determine whether excitatory rTMS can enhance SPiN in younger and elderly adults via stimulation of the left pSTS and/or left PMv. We hypothesized that performance gain would be more limited in older compared to younger adults because of known reduced plasticity in the aging brain. An effect of target (pSTS, PMv) would suggest that one region has a stronger functional contribution to SPiN and might represent a better option to reduce or prevent SPiN decline in aging using non-invasive brain stimulation.

Section snippets

Participants

22 healthy native Canadian French speakers were recruited through the laboratory database, emails, posts on the lab website (www.speechneurolab.ca), lab Facebook page (https://www.facebook.com/speechneurolab/) and flyers distributed in various institutions, including shops and retirement homes throughout Québec City. One participant was excluded from the analyses due to inability to complete the main task. The remaining participants were aged 20–85 years (mean 53.33 ± 20.52 years). A telephone

Participants

A sample of 34 healthy right-handed healthy native French speakers aged 32–79 years (M = 57.35, SD = 14.69) was recruited through emails sent to the university community and the Centre intégré universitaire de santé et des services sociaux de la Capitale-Nationale, posts on the lab website (www.speechneurolab.ca) and Facebook page (https://www.facebook.com/speechneurolab/) and flyers distributed in various institutions, including shops and retirement homes throughout Québec City, as well as

Discussion

The objectives of this study were to determine if SPiN performance in young and older adults can be enhanced by excitatory rTMS to two areas involved in processing sublexical speech (i.e., the left pSTS, and the left PMv). To achieve this goal, we created a reliable syllable discrimination task. The results of Experiments 1 show that older adults are less accurate in our syllable discrimination task. In Experiment 2, we found this same age effect on accuracy in the baseline condition, which

Limitations

One potential limitation of this experiment was that TMS sessions were delivered on the same day. While this design has the advantage of eliminating variability related to the participant’s health, mood and state of mind during the administration of the tests, the TMS effects could have interacted (i.e., spillover effect). We controlled for this by 1) adding a delay of at least 60 min after a real stimulation before performing a second session (e.g. Chung, Hill, Rogasch, Hoy, & Fitzgerald, 2016

Conclusion

Our TMS study is the first to show that hugely prevalent age-related SPiN difficulties can be reduced by enhancing cortical excitability within the speech-processing network, especially when targeting the left PMv. Importantly, initial performance—not age—was the main driving factor for TMS-induced performance improvement. This study paves the way for the development of approaches to enhance speech processing using neurostimulation methods. Future studies are needed to determine how to maximize

Funding

This work was supported by P.T.’s grants from the Natural Sciences and Engineering Research Council of Canada [RGPIN-2019-06534] and the Canadian Foundation for Innovation [31408]. P.T. also holds a Career Awards from the “Fonds de Recherche du Québec – Santé” (FRQS) [35016]. V.B. was supported by fellowships from the CERVO foundation and from Université Laval (Department of Rehabilitation).

CRediT authorship contribution statement

Valérie Brisson: Conceptualization, Methodology, Investigation, Project administration, Formal analysis, Visualization, Writing - original draft, Data curation. Pascale Tremblay: Conceptualization, Funding acquisition, Methodology, Investigation, Supervision, Resources, Project administration, Writing - review & editing, Data curation.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We thank all participants. Thanks also to Maxime Perron for his precious help developing the stimuli and task, to Audrey Desjardins and Alison Arseneault for their contribution to participant recruitment and data collection, and to Catherine Fontaine-Lavallée for administrative support.

References (113)

  • G. Hickok

    The cortical organization of speech processing: Feedback control and predictive coding the context of a dual-stream model

    Journal of Communication Disorders

    (2012)
  • M.R. Hinder et al.

    Inter- and Intra-individual variability following intermittent theta burst stimulation: Implications for rehabilitation and recovery

    Brain Stimul

    (2014)
  • Y.Z. Huang et al.

    Theta burst stimulation of the human motor cortex

    Neuron

    (2005)
  • S. Kim et al.

    Effect of age on binaural speech intelligibility in normal hearing adults

    Speech Communication

    (2006)
  • E. Liebenthal et al.

    An interactive model of auditory-motor speech perception

    Brain and Language

    (2018)
  • V. López-Alonso et al.

    Inter-individual variability in response to non-invasive brain stimulation paradigms

    Brain Stimul

    (2014)
  • J. Lüdemann-Podubecká et al.

    Repetitive transcranial magnetic stimulation for motor recovery of the upper limb after stroke

    Progress in Brain Research

    (2015)
  • I.G. Meister et al.

    The essential role of premotor cortex in speech perception

    Current Biology: CB

    (2007)
  • H.E. Nuttall et al.

    Modulation of intra- and inter-hemispheric connectivity between primary and premotor cortex during speech perception

    Brain and Language

    (2018)
  • R.C. Oldfield

    The assessment and analysis of handedness: The Edinburgh inventory

    Neuropsychologia

    (1971)
  • M.T.N. Panouilleres et al.

    Decline of auditory-motor speech processing in older adults with hearing loss

    Neurobiology of Aging

    (2018)
  • J. Restle et al.

    Facilitation of speech repetition accuracy by theta burst stimulation of the left posterior inferior frontal gyrus

    Neuropsychologia

    (2012)
  • S. Rossi et al.

    Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research

    Clinical Neurophysiology

    (2009)
  • K.S. Rufener et al.

    Transcranial Alternating Current Stimulation (tACS) differentially modulates speech perception in young and older adults

    Brain Stimulation

    (2016)
  • M. Sato et al.

    A mediating role of the premotor cortex in phoneme segmentation

    Brain and Language

    (2009)
  • J.I. Skipper et al.

    The hearing ear is always found close to the speaking tongue: Review of the role of the motor system in speech perception

    Brain and Language

    (2017)
  • P. Tremblay et al.

    Brain aging and speech perception: Effects of background noise and talker variability

    Neuroimage

    (2021)
  • P. Tremblay et al.

    On the context-dependent nature of the contribution of the ventral premotor cortex to speech perception

    Neuroimage

    (2011)
  • C. Alain et al.

    Listening under difficult conditions: An activation likelihood estimation meta-analysis

    Human Brain Mapping

    (2018)
  • S. Anderson et al.

    A neural basis of speech-in-noise perception in older adults

    Ear and Hearing

    (2011)
  • J. Aydelott et al.

    Normal adult aging and the contextual influences affecting speech and meaningful sound perception

    Trends in Amplification

    (2010)
  • M.S. Beauchamp et al.

    fMRI-guided transcranial magnetic stimulation reveals that the superior temporal sulcus is a cortical locus of the McGurk effect

    The Journal of Neuroscience

    (2010)
  • P. Bédard et al.

    SyllabO+: A new tool to study sublexical phenomena in spoken Quebec French

    Behavior Research Methods

    (2017)
  • J. Benichov et al.

    Word recognition within a linguistic context: Effects of age, hearing acuity, verbal ability, and cognitive function

    Ear and Hearing

    (2012)
  • T. Bever et al.

    Analysis by synthesis: A (Re-)emerging program of research for language and vision

    Biolinguistics

    (2010)
  • M. Bilodeau-Mercure et al.

    The neurobiology of speech perception decline in aging

    Brain Structure & Function

    (2015)
  • Boersma, P., & Weenink, D. (2011). Praat: Doing phonetics by computer (Version 6.0). Amsterdam, the Netherlands:...
  • Caron, H. (Producer). (2007). Entendez-vous bien [Measurement instrument]. Retrieved from...
  • T.K. Chao et al.

    Predictive model for progression of hearing loss: Meta-analysis of multi-state outcome

    Journal of Evaluation in Clinical Practice

    (2009)
  • J.J. Chen et al.

    Association of central noninvasive brain stimulation interventions with efficacy and safety in tinnitus management: A meta-analysis

    JAMA Otolaryngol Head Neck Surg

    (2020)
  • J. Cohen

    Statistical power analysis

    Current Directions in Psychological Science

    (1992)
  • J.T. Devlin et al.

    Stimulating language: Insights from TMS

    Brain

    (2007)
  • D.S.E. Dickins et al.

    Plasticity induced by intermittent theta burst stimulation in bilateral motor cortices is not altered in older adults

    Neural Plasticity

    (2015)
  • Y. Du et al.

    Increased activity in frontal motor cortex compensates impaired speech perception in older adults

    Nature Communications

    (2016)
  • J.R. Dubno et al.

    Longitudinal changes in speech recognition in older persons

    Journal of the Acoustical Society of America

    (2008)
  • M.A. Eckert et al.

    Auditory cortex signs of age-related hearing loss

    Journal of the Association for Research in Otolaryngology

    (2012)
  • M.A. Eckert et al.

    Is Listening in noise worth it? The neurobiology of speech recognition in challenging listening conditions

    Ear and hearing

    (2016)
  • M.A. Eckert et al.

    Age-related effects on word recognition: Reliance on cognitive control systems with structural declines in speech-responsive cortex

    Journal of the Association for Research in Otolaryngology: JARO

    (2008)
  • L.J. Edwards et al.

    An R2 statistic for fixed effects in the linear mixed model

    Statistics in Medicine

    (2008)
  • S. Finkel et al.

    Intermittent theta burst stimulation over right somatosensory larynx cortex enhances vocal pitch-regulation in nonsingers

    Human Brain Mapping

    (2019)
  • View full text