The Cingulo-Opercular Network Provides Word-Recognition Benefit

Recognizing speech in difficult listening conditions requires considerable focus of attention that is often demonstrated by elevated activity in putative attention systems, including the cingulo-opercular network. We tested the prediction that elevated cingulo-opercular activity provides word-recognition benefit on a subsequent trial. Eighteen healthy, normal-hearing adults (10 females; aged 20–38 years) performed word recognition (120 trials) in multi-talker babble at +3 and +10 dB signal-to-noise ratios during a sparse sampling functional magnetic resonance imaging (fMRI) experiment. Blood oxygen level-dependent (BOLD) contrast was elevated in the anterior cingulate cortex, anterior insula, and frontal operculum in response to poorer speech intelligibility and response errors. These brain regions exhibited significantly greater correlated activity during word recognition compared with rest, supporting the premise that word-recognition demands increased the coherence of cingulo-opercular network activity. Consistent with an adaptive control network explanation, general linear mixed model analyses demonstrated that increased magnitude and extent of cingulo-opercular network activity was significantly associated with correct word recognition on subsequent trials. These results indicate that elevated cingulo-opercular network activity is not simply a reflection of poor performance or error but also supports word recognition in difficult listening conditions.

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

[2]  Mark Laubach,et al.  Working with memory: evidence for a role for the medial prefrontal cortex in performance monitoring during spatial delayed alternation. , 2012, Journal of neurophysiology.

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

[4]  Matthew H. Davis,et al.  Brain regions recruited for the effortful comprehension of noise-vocoded words , 2012 .

[5]  Richard H. Wilson,et al.  The effects of energetic and informational masking on The Words-in-Noise Test (WIN). , 2012, Journal of the American Academy of Audiology.

[6]  Patti Adank,et al.  The neural bases of difficult speech comprehension and speech production: Two Activation Likelihood Estimation (ALE) meta-analyses , 2012, Brain and Language.

[7]  Stefanie E. Kuchinsky,et al.  Word intelligibility and age predict visual cortex activity during word listening. , 2012, Cerebral cortex.

[8]  Stefanie E. Kuchinsky,et al.  Multiple imputation of missing fMRI data in whole brain analysis , 2012, NeuroImage.

[9]  Marko Wilke,et al.  An alternative approach towards assessing and accounting for individual motion in fMRI timeseries , 2012, NeuroImage.

[10]  Matthew H. Davis,et al.  Neural dissociation in processing noise and accent in spoken language comprehension , 2012, Neuropsychologia.

[11]  Ferath Kherif,et al.  Does Semantic Context Benefit Speech Understanding through “Top–Down” Processes? Evidence from Time-resolved Sparse fMRI , 2011, Journal of Cognitive Neuroscience.

[12]  M. Ullsperger,et al.  Post-Error Adjustments , 2011, Front. Psychology.

[13]  Tom Eichele,et al.  Posterior Medial Frontal Cortex Activity Predicts Post-Error Adaptations in Task-Related Visual and Motor Areas , 2011, The Journal of Neuroscience.

[14]  Jonathan H. Venezia,et al.  Hierarchical organization of human auditory cortex: evidence from acoustic invariance in the response to intelligible speech. , 2010, Cerebral cortex.

[15]  Franziska M. Korb,et al.  Post-Error Behavioral Adjustments Are Facilitated by Activation and Suppression of Task-Relevant and Task-Irrelevant Information Processing , 2010, The Journal of Neuroscience.

[16]  Gregory Hickok,et al.  Phonological repetition-suppression in bilateral superior temporal sulci , 2010, NeuroImage.

[17]  Joseph T. Devlin,et al.  On-line plasticity in spoken sentence comprehension: Adapting to time-compressed speech , 2010, NeuroImage.

[18]  A. Kleinschmidt,et al.  Distributed and Antagonistic Contributions of Ongoing Activity Fluctuations to Auditory Stimulus Detection , 2009, The Journal of Neuroscience.

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

[20]  M. Eckert,et al.  Speech Recognition in Younger and Older Adults: A Dependency on Low-Level Auditory Cortex , 2009, The Journal of Neuroscience.

[21]  K. R. Ridderinkhof,et al.  Medial frontal cortex and response conflict: Evidence from human intracranial EEG and medial frontal cortex lesion , 2008, Brain Research.

[22]  Jonas Obleser,et al.  Bilateral Speech Comprehension Reflects Differential Sensitivity to Spectral and Temporal Features , 2008, The Journal of Neuroscience.

[23]  T. Parrish,et al.  Cortical mechanisms of speech perception in noise. , 2008, Journal of speech, language, and hearing research : JSLHR.

[24]  Kenneth Hugdahl,et al.  Prediction of human errors by maladaptive changes in event-related brain networks , 2008, Proceedings of the National Academy of Sciences.

[25]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

[26]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[27]  Jonathan Berger,et al.  Neural Dynamics of Event Segmentation in Music: Converging Evidence for Dissociable Ventral and Dorsal Networks , 2007, Neuron.

[28]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[29]  S. Scott,et al.  Functional Integration across Brain Regions Improves Speech Perception under Adverse Listening Conditions , 2007, The Journal of Neuroscience.

[30]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

[31]  Adriana A. Zekveld,et al.  Top–down and bottom–up processes in speech comprehension , 2006, NeuroImage.

[32]  Jason R. Tregellas,et al.  Effect of task difficulty on the functional anatomy of temporal processing , 2006, NeuroImage.

[33]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[34]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[35]  Gereon R. Fink,et al.  Using fMRI to decompose the neural processes underlying the Wisconsin Card Sorting Test , 2006, NeuroImage.

[36]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[37]  S. Scott,et al.  The neural correlates of declining performance with age: evidence for age-related changes in cognitive control. , 2005, Cerebral cortex.

[38]  P. Hagoort.  On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

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

[40]  Willy Serniclaes,et al.  Neural correlates of switching from auditory to speech perception , 2005, NeuroImage.

[41]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

[42]  J. Gee,et al.  Geodesic estimation for large deformation anatomical shape averaging and interpolation , 2004, NeuroImage.

[43]  D. Yves von Cramon,et al.  Neuroimaging of Performance Monitoring: Error Detection and Beyond , 2004, Cortex.

[44]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[45]  Clay B. Holroyd,et al.  Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance , 2004, Neuroscience & Biobehavioral Reviews.

[46]  D. V. von Cramon,et al.  Neural correlates of error detection and error correction: is there a common neuroanatomical substrate? , 2004, The European journal of neuroscience.

[47]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[48]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[49]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

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

[51]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[52]  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.

[53]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  G I de Zubicaray,et al.  The semantic interference effect in the picture‐word paradigm: An event‐related fMRI study employing overt responses , 2001, Human brain mapping.

[55]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[56]  R. Poldrack,et al.  Relations between the Neural Bases of Dynamic Auditory Processing and Phonological Processing: Evidence from fMRI , 2001, Journal of Cognitive Neuroscience.

[57]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[58]  D. Dirks,et al.  Examination of the Neighborhood Activation Theory in Normal and Hearing-Impaired Listeners , 2001, Ear and hearing.

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

[60]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[61]  S. Blumstein,et al.  The Role of Segmentation in Phonological Processing: An fMRI Investigation , 2000, Journal of Cognitive Neuroscience.

[62]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[63]  D. Hofmann.  An Overview of the Logic and Rationale of Hierarchical Linear Models , 1997 .

[64]  M. Posner,et al.  Localization of a Neural System for Error Detection and Compensation , 1994 .

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

[66]  L L Elliott,et al.  Development of a test of speech intelligibility in noise using sentence materials with controlled word predictability. , 1977, The Journal of the Acoustical Society of America.

[67]  A. B. Hollingshead,et al.  Four factor index of social status , 1975 .

[68]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[69]  T W Tillman,et al.  Perceptual masking in multiple sound backgrounds. , 1969, The Journal of the Acoustical Society of America.

[70]  G. A. Miller,et al.  The masking of speech. , 1947, Psychological bulletin.