Articulation-based sound perception in verbal repetition: a functional NIRS study

Verbal repetition is a fundamental language capacity where listening and speaking are inextricably coupled with each other. We have recently reported that the left inferior frontal gyrus (IFG) harbors articulation-based codes, as evidenced by activation during repetition of meaningless speech sounds, i.e., pseudowords. In this study, we aimed at confirming this finding and further investigating the possibility that sound perception as well as articulation is subserved by neural circuits in this region. Using functional near-infrared spectroscopy (fNIRS), we monitored changes of hemoglobin (Hb) concentration at IFG bilaterally, while subjects verbally repeated pseudowords and words. The results revealed that the proportion of oxygenated hemoglobin (O2Hb) over total Hb was significantly higher at the left IFG during repetition of pseudowords than that of words, replicating the observation by functional MRI and indicating that the region processes articulatory codes for verbal repetition. More importantly for this study, hemodynamic modulations were observed at both IFG during passive listening without repetition to various sounds, including natural environmental sounds, animal vocalizations, and human non-speech sounds. Furthermore, the O2Hb concentration increased at the left IFG but decreased at the right IFG for both speech and non-speech sounds. These findings suggest that both speech and non-speech sounds may be processed and maintained by a neural mechanism for sensorimotor integration using articulatory codes at the left IFG.

[1]  G. A. Miller.  THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[2]  G. Crelier,et al.  Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  S. Scott,et al.  Positive Emotions Preferentially Engage an Auditory–Motor “Mirror” System , 2006, The Journal of Neuroscience.

[4]  Alan R. Palmer,et al.  The Oxford Handbook of Auditory Science: The Auditory Brain , 2010 .

[5]  David A. Boas,et al.  A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans , 2006, NeuroImage.

[6]  Marco Iacoboni,et al.  Neural responses to non-native phonemes varying in producibility: Evidence for the sensorimotor nature of speech perception , 2006, NeuroImage.

[7]  I. Kanno,et al.  Changes in CBF and CBV during changes in neural activity or PaCO2 measured by PET , 2004 .

[8]  Julio Acosta-Cabronero,et al.  Social cognitive deficits and their neural correlates in progressive supranuclear palsy , 2012, Brain : a journal of neurology.

[9]  John Coleman,et al.  Cognitive reality and the phonological lexicon: A review , 1998, Journal of Neurolinguistics.

[10]  R. Ingham,et al.  Stuttered and fluent speech production: An ALE meta‐analysis of functional neuroimaging studies , 2005, Human brain mapping.

[11]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[12]  Anne-Lise Giraud,et al.  How the brain repairs stuttering. , 2009, Brain : a journal of neurology.

[13]  S. Sato,et al.  Developmental changes of cerebral blood flow and oxygen metabolism in children. , 1999, AJNR. American journal of neuroradiology.

[14]  B. C. Griffith,et al.  The discrimination of speech sounds within and across phoneme boundaries. , 1957, Journal of experimental psychology.

[15]  T. Hackett,et al.  Structural organization of the ascending auditory pathway , 2010 .

[16]  M. Iacoboni,et al.  Listening to speech activates motor areas involved in speech production , 2004, Nature Neuroscience.

[17]  Sophie K. Scott,et al.  Brain mechanisms for processing perceived emotional vocalizations in humans , 2009 .

[18]  D. Delpy,et al.  Measurement of CMRO2 in neonates undergoing intensive care using near infrared spectroscopy. , 2005, Advances in experimental medicine and biology.

[19]  G. Rizzolatti,et al.  Speech listening specifically modulates the excitability of tongue muscles: a TMS study , 2002, The European journal of neuroscience.

[20]  S. Scott,et al.  Inferior Frontal Gyrus Activation Predicts Individual Differences in Perceptual Learning of Cochlear-Implant Simulations , 2010, The Journal of Neuroscience.

[21]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[22]  E. Okada,et al.  Monte Carlo prediction of near-infrared light propagation in realistic adult and neonatal head models. , 2003, Applied optics.

[23]  D. Massaro.  Speech Perception By Ear and Eye: A Paradigm for Psychological Inquiry , 1989 .

[24]  J. Mazziotta,et al.  Cracking the Language Code: Neural Mechanisms Underlying Speech Parsing , 2006, The Journal of Neuroscience.

[25]  N. Logothetis.  The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  P. Kuhl.  Early language acquisition: cracking the speech code , 2004, Nature Reviews Neuroscience.

[27]  D. Delpy,et al.  COTSIDE MEASUREMENT OF CEREBRAL BLOOD FLOW IN ILL NEWBORN INFANTS BY NEAR INFRARED SPECTROSCOPY , 1988, The Lancet.

[28]  W. Marslen-Wilson.  Functional parallelism in spoken word-recognition , 1987, Cognition.

[29]  R. Poldrack,et al.  Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy? , 2003, Physics in medicine and biology.

[30]  A. Caramazza,et al.  Dissociation of algorithmic and heuristic processes in language comprehension: Evidence from aphasia , 1976, Brain and Language.

[31]  A. Braun,et al.  Comparison of continuous overt speech fMRI using BOLD and arterial spin labeling , 2005, Human brain mapping.

[32]  Reinhold Orglmeister,et al.  Automatic analysis of systolic, diastolic and mean blood pressure of continuous measurement before, during and after sleep arousals in polysomnographic overnight recordings , 2012 .

[33]  S. Grimm,et al.  Novelty Detection in the Human Auditory Brainstem , 2012, The Journal of Neuroscience.

[34]  D. Delpy,et al.  System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination , 1988, Medical and Biological Engineering and Computing.

[35]  K. Schmidt,et al.  Differential responses in CBF and CBV to cocaine as measured by fMRI: implications for pharmacological MRI signals derived oxygen metabolism assessment. , 2009, Journal of psychiatric research.

[36]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[37]  Friedemann Pulvermüller,et al.  Motor cortex maps articulatory features of speech sounds , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  C. Fowler.  An event approach to the study of speech perception from a direct realist perspective , 1986 .

[39]  Ting-Yim Lee,et al.  Near-Infrared Spectroscopy Measurement of Oxygen Extraction Fraction and Cerebral Metabolic Rate of Oxygen in Newborn Piglets , 2003, Pediatric Research.

[40]  G. Vingerhoets,et al.  Results of a pilot study on the involvement of bilateral inferior frontal gyri in emotional prosody perception: an rTMS study , 2010, BMC Neuroscience.

[41]  K. Müller,et al.  Functional architecture of verbal and tonal working memory: An FMRI study , 2009, Human brain mapping.

[42]  S. Nicolson,et al.  Arterial and Venous Contributions to Near-infrared Cerebral Oximetry , 2000, Anesthesiology.

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

[44]  J. Detre,et al.  Technical aspects and utility of fMRI using BOLD and ASL , 2002, Clinical Neurophysiology.

[45]  M. Iacoboni.  Neural mechanisms of imitation , 2005, Current Opinion in Neurobiology.

[46]  Z. Cho,et al.  Dual routes for verbal repetition: Articulation-based and acoustic–phonetic codes for pseudoword and word repetition, respectively , 2012, Brain and Language.

[47]  Eduardo Miranda,et al.  Modelling the Development of Mirror Neurons for Auditory-Motor Integration , 2002 .

[48]  A. Liberman,et al.  The motor theory of speech perception revised , 1985, Cognition.

[49]  J Marshall,et al.  In vivo Measurement of Regional Cerebral Haematocrit Using Positron Emission Tomography , 1984, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[50]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[51]  Kenneth Hugdahl,et al.  Stimulus expectancy modulates inferior frontal gyrus and premotor cortex activity in auditory perception , 2012, Brain and Language.