Differences in Hearing Acuity among “Normal-Hearing” Young Adults Modulate the Neural Basis for Speech Comprehension

Abstract In this paper, we investigate how subtle differences in hearing acuity affect the neural systems supporting speech processing in young adults. Auditory sentence comprehension requires perceiving a complex acoustic signal and performing linguistic operations to extract the correct meaning. We used functional MRI to monitor human brain activity while adults aged 18–41 years listened to spoken sentences. The sentences varied in their level of syntactic processing demands, containing either a subject-relative or object-relative center-embedded clause. All participants self-reported normal hearing, confirmed by audiometric testing, with some variation within a clinically normal range. We found that participants showed activity related to sentence processing in a left-lateralized frontotemporal network. Although accuracy was generally high, participants still made some errors, which were associated with increased activity in bilateral cingulo-opercular and frontoparietal attention networks. A whole-brain regression analysis revealed that activity in a right anterior middle frontal gyrus (aMFG) component of the frontoparietal attention network was related to individual differences in hearing acuity, such that listeners with poorer hearing showed greater recruitment of this region when successfully understanding a sentence. The activity in right aMFGs for listeners with poor hearing did not differ as a function of sentence type, suggesting a general mechanism that is independent of linguistic processing demands. Our results suggest that even modest variations in hearing ability impact the systems supporting auditory speech comprehension, and that auditory sentence comprehension entails the coordination of a left perisylvian network that is sensitive to linguistic variation with an executive attention network that responds to acoustic challenge.

[1]  Mark A. Eckert,et al.  Cingulo-opercular activity affects incidental memory encoding for speech in noise , 2017, NeuroImage.

[2]  F. Lin,et al.  Addressing Estimated Hearing Loss in Adults in 2060 , 2017, JAMA otolaryngology-- head & neck surgery.

[3]  J. Peelle Listening Effort: How the Cognitive Consequences of Acoustic Challenge Are Reflected in Brain and Behavior , 2017, Ear and hearing.

[4]  A. Wingfield,et al.  Effort Not Speed Characterizes Comprehension of Spoken Sentences by Older Adults with Mild Hearing Impairment , 2017, Front. Aging Neurosci..

[5]  A. Wingfield,et al.  The Neural Consequences of Age-Related Hearing Loss , 2016, Trends in Neurosciences.

[6]  A. Wingfield,et al.  Hearing Impairment and Cognitive Energy: The Framework for Understanding Effortful Listening (FUEL) , 2016, Ear and hearing.

[7]  A. Wingfield,et al.  Acoustic richness modulates the neural networks supporting intelligible speech processing , 2016, Hearing Research.

[8]  A. Wingfield,et al.  The Two Sides of Sensory–Cognitive Interactions: Effects of Age, Hearing Acuity, and Working Memory Span on Sentence Comprehension , 2016, Front. Psychol..

[9]  Chad S. Rogers,et al.  Effects of Age, Acoustic Challenge, and Verbal Working Memory on Recall of Narrative Speech , 2016, Experimental aging research.

[10]  A. Wingfield,et al.  Cognitive aging and hearing acuity: modeling spoken language comprehension , 2015, Front. Psychol..

[11]  Stefanie E. Kuchinsky,et al.  Cortical Activity Predicts Which Older Adults Recognize Speech in Noise and When , 2015, The Journal of Neuroscience.

[12]  Joseph W. Dubis,et al.  Spatial and Temporal Characteristics of Error-Related Activity in the Human Brain , 2015, The Journal of Neuroscience.

[13]  Jonathan E. Peelle,et al.  Methodological challenges and solutions in auditory functional magnetic resonance imaging , 2014, Front. Neurosci..

[14]  A. Wingfield,et al.  Acoustic masking disrupts time-dependent mechanisms of memory encoding in word-list recall , 2014, Memory & cognition.

[15]  A. Zekveld,et al.  Cognitive processing load across a wide range of listening conditions: insights from pupillometry. , 2014, Psychophysiology.

[16]  Stefanie E. Kuchinsky,et al.  The Cingulo-Opercular Network Provides Word-Recognition Benefit , 2013, The Journal of Neuroscience.

[17]  T. Lunner,et al.  The Ease of Language Understanding (ELU) model: theoretical, empirical, and clinical advances , 2013, Front. Syst. Neurosci..

[18]  Jonas Obleser,et al.  The Brain Dynamics of Rapid Perceptual Adaptation to Adverse Listening Conditions , 2013, The Journal of Neuroscience.

[19]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[20]  Satrajit S. Ghosh,et al.  Optimized Design and Analysis of Sparse-Sampling fMRI Experiments , 2013, Front. Neurosci..

[21]  Jonathan D. Power,et al.  Control-related systems in the human brain , 2013, Current Opinion in Neurobiology.

[22]  Jonathan E. Peelle,et al.  The hemispheric lateralization of speech processing depends on what “speech” is: a hierarchical perspective , 2012, Front. Hum. Neurosci..

[23]  Patti Adank,et al.  Design choices in imaging speech comprehension: An Activation Likelihood Estimation (ALE) meta-analysis , 2012, NeuroImage.

[24]  Matthew H. Davis,et al.  Effortful Listening: The Processing of Degraded Speech Depends Critically on Attention , 2012, The Journal of Neuroscience.

[25]  Sophie K. Scott,et al.  An Application of Univariate and Multivariate Approaches in fMRI to Quantifying the Hemispheric Lateralization of Acoustic and Linguistic Processes , 2012, Journal of Cognitive Neuroscience.

[26]  Angela D Friederici,et al.  The language network , 2012, Current Opinion in Neurobiology.

[27]  Jean-Pierre Gagné,et al.  Older adults expend more listening effort than young adults recognizing audiovisual speech in noise , 2011, International journal of audiology.

[28]  J. Duncan,et al.  Adaptive Coding of Task-Relevant Information in Human Frontoparietal Cortex , 2011, The Journal of Neuroscience.

[29]  Sophie K. Scott,et al.  Hemispheric Asymmetries in Speech Perception: Sense, Nonsense and Modulations , 2011, PloS one.

[30]  A. Wingfield,et al.  Hearing Loss in Older Adults Affects Neural Systems Supporting Speech Comprehension , 2011, The Journal of Neuroscience.

[31]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[32]  J. Hall,et al.  Evidence of hearing loss in a ‘normally-hearing’ college-student population , 2011, International journal of audiology.

[33]  J. Gee,et al.  Why are patients with progressive nonfluent aphasia nonfluent? , 2010, Neurology.

[34]  Matthew H. Davis,et al.  Hierarchical Processing for Speech in Human Auditory Cortex and Beyond , 2010, Front. Hum. Neurosci..

[35]  J. Duncan,et al.  Lateral Prefrontal Cortex Subregions Make Dissociable Contributions during Fluid Reasoning , 2010, Cerebral cortex.

[36]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[37]  A. Wingfield,et al.  Neural processing during older adults' comprehension of spoken sentences: age differences in resource allocation and connectivity. , 2010, Cerebral cortex.

[38]  A. Wingfield,et al.  Aging, hearing acuity, and the attentional costs of effortful listening. , 2009, Psychology and aging.

[39]  Adam R. Walczak,et al.  At the heart of the ventral attention system: The right anterior insula , 2009, Human brain mapping.

[40]  B. Fligor Personal listening devices and hearing loss: seeking evidence of a long term problem through a successful short-term investigation. , 2009, Noise & health.

[41]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[42]  A E Holmes,et al.  Hearing, use of hearing protection, and attitudes towards noise among young American adults , 2009, International journal of audiology.

[43]  Bruce A. Schneider,et al.  Investigating the Influence of Continuous Babble on Auditory Short-Term Memory Performance , 2008, Quarterly journal of experimental psychology.

[44]  Adam R. Walczak,et al.  Age-related Effects on Word Recognition: Reliance on Cognitive Control Systems with Structural Declines in Speech-responsive Cortex , 2008, Journal of the Association for Research in Otolaryngology.

[45]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[46]  Arthur Wingfield,et al.  Effects of adult aging and hearing loss on comprehension of rapid speech varying in syntactic complexity. , 2006, Journal of the American Academy of Audiology.

[47]  Ingrid S. Johnsrude,et al.  Interleaved silent steady state (ISSS) imaging: A new sparse imaging method applied to auditory fMRI , 2006, NeuroImage.

[48]  Matthias Schlesewsky,et al.  Processing linguistic complexity and grammaticality in the left frontal cortex. , 2005, Cerebral cortex.

[49]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[50]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[51]  A. Wingfield,et al.  Hearing Loss in Older Adulthood , 2005 .

[52]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[53]  Arthur Wingfield,et al.  Hearing Loss and Perceptual Effort: Downstream Effects on Older Adults’ Memory for Speech , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[54]  Murray Grossman,et al.  Dissociable patterns of brain activity during comprehension of rapid and syntactically complex speech: Evidence from fMRI , 2004, Brain and Language.

[55]  Weijia Ni,et al.  Sentence complexity and input modality effects in sentence comprehension: an fMRI study , 2004, NeuroImage.

[56]  Matthew H. Davis,et al.  Hierarchical Processing in Spoken Language Comprehension , 2003, The Journal of Neuroscience.

[57]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

[58]  J. Gee,et al.  Neural basis for sentence comprehension: Grammatical and short‐term memory components , 2002, Human brain mapping.

[59]  Erica B. Michael,et al.  fMRI investigation of sentence comprehension by eye and by ear: Modality fingerprints on cognitive processes , 2001, Human brain mapping.

[60]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[61]  R. Klein,et al.  Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study. , 1998, American journal of epidemiology.

[62]  J M Festen,et al.  Assessing aspects of auditory handicap by means of pupil dilatation. , 1997, Audiology : official organ of the International Society of Audiology.

[63]  C. Meyer-Bisch,et al.  Epidemiological evaluation of hearing damage related to strongly amplified music (personal cassette players, discotheques, rock concerts)--high-definition audiometric survey on 1364 subjects. , 1996, Audiology : official organ of the International Society of Audiology.

[64]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[65]  P. Carpenter,et al.  Individual differences in working memory and reading , 1980 .

[66]  P. Rabbitt,et al.  Channel-Capacity, Intelligibility and Immediate Memory , 1968, The Quarterly journal of experimental psychology.

[67]  Stefanie E. Kuchinsky,et al.  Pupil size varies with word listening and response selection difficulty in older adults with hearing loss. , 2013, Psychophysiology.

[68]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[69]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.