Human brain activation during phonation and exhalation: common volitional control for two upper airway functions
Open accessAbstract
Phonation is defined as a laryngeal motor behavior used for speech production, which involves a highly specialized coordination of laryngeal and respiratory neuromuscular control. During speech, brief periods of vocal fold vibration for vowels are interspersed by voiced and unvoiced consonants, glottal stops and glottal fricatives (/h/). It remains unknown whether laryngeal/respiratory coordination of phonation for speech relies on separate neural systems from respiratory control or whether a common system controls both behaviors. To identify the central control system for human phonation, we used event-related fMRI to contrast brain activity during phonation with activity during prolonged exhalation in healthy adults. Both whole-brain analyses and region of interest comparisons were conducted. Production of syllables containing glottal stops and vowels was accompanied by activity in left sensorimotor, bilateral temporoparietal and medial motor areas. Prolonged exhalation similarly involved activity in left sensorimotor and temporoparietal areas but not medial motor areas. Significant differences between phonation and exhalation were found primarily in the bilateral auditory cortices with whole-brain analysis. The ROI analysis similarly indicated task differences in the auditory cortex with differences also detected in the inferolateral motor cortex and dentate nucleus of the cerebellum. A second experiment confirmed that activity in the auditory cortex only occurred during phonation for speech and did not depend upon sound production. Overall, a similar central neural system was identified for both speech phonation and voluntary exhalation that primarily differed in auditory monitoring.
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Phonation contributes to activation in bilateral sensorimotor cortex during articulation.
“The contribution of phonation to activation in the bilateral sensorimotor cortex during articulation was also emphasized in several studies (Loucks et al., 2007; Brown et al., 2008, 2009; Grabski et al., 2011; Simonyan et al., 2009; Simonyan and Horwitz, 2011).”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Loucks et al., 2007
In SMA-proper, activation is greater for complex articulation than prolonged vowel production or exhalation and is maintained during production, consistent with a role in execution as well as initiation.
“In the SMA-proper, activation was greater for complex articulation than prolonged vowel production or exhalation (Loucks et al., 2007) and maintained during production consistent with a role in execution as well as initiation (Brendel et al., 2010).”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Loucks et al., 2007
Bilateral insula regions are involved in phonation for speech, volitional exhalation, and syllable singing.
“This is consistent with observations that bilateral insula regions are involved in phonation for speech, volitional exhalation (Loucks et al., 2007) and syllable singing (Brown et al., 2009; Zarate et al., 2010).”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Loucks et al., 2007
Posterior medial dorsal surface of superior temporal gyri, including planum temporale, is activated during repetitive (silent) movements of jaw and tongue as well as during auditory feedback and nonspeech vocal tract movements.
“Fifth, the posterior medial dorsal surface of the superior temporal gyri, including the planum temporale, were found to be activated during repetitive (silent) movements of the jaw and tongue as well as during auditory feedback (Dhanjal et al., 2008) and nonspeech vocal tract movements (Loucks et al., 2007).”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Loucks et al., 2007
Cites
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
(1960) · Medical Journal of Australia · doi:10.5694/j.1326-5377.1960.tb76238.x · Cited by 2,178 · see citing works
<i>Principles of Voice Production</i>
Titze, I. R., & Martin, D. W. (1998) · The Journal of the Acoustical Society of America · doi:10.1121/1.424266 · Cited by 1,643 · see citing works
Meta-analysis of the functional neuroanatomy of single-word reading: method and validation
Turkeltaub, P. E., Eden, G. F., Jones, K. M., & Zeffiro, T. A. (2002) · NeuroImage · doi:10.1006/nimg.2002.1131 · Cited by 1,604 · see citing works
Supplementary motor area structure and function: Review and hypotheses
Goldberg, G. (1985) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00045167 · Cited by 1,229 · see citing works
Neural modeling and imaging of the cortical interactions underlying syllable production
Guenther, F. H., Ghosh, S. S., & Tourville, J. A. (2006) · Brain and Language · doi:10.1016/j.bandl.2005.06.001 · Cited by 879 · see citing works
Neural pathways underlying vocal control
Jürgens, U. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00068-9 · Cited by 846 · see citing works
Handbook of clinical audiology
Katz, J. L. (1978) · Cited by 604 · see citing works
Handbook of Clinical Audiology.
Sanders, J. W. (1986) · Ear and Hearing · doi:10.1097/00003446-198608000-00010 · Cited by 594 · see citing works
An fMRI investigation of syllable sequence production
Bohland, J. W., & Guenther, F. H. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.04.173 · Cited by 545 · see citing works
Brain regions involved in articulation
Wise, R., Greene, J., Büchel, C., & Scott, S. (1999) · The Lancet · doi:10.1016/s0140-6736(98)07491-1 · Cited by 517 · see citing works
Voice F0 responses to manipulations in pitch feedback
Burnett, T. A., Freedland, M. B., Larson, C. R., & Hain, T. C. (1998) · The Journal of the Acoustical Society of America · doi:10.1121/1.423073 · Cited by 508 · see citing works
Human temporal-lobe response to vocal sounds
Belin, P., Zatorre, R. J., & Ahad, P. (2002) · Cognitive Brain Research · doi:10.1016/s0926-6410(01)00084-2 · Cited by 452 · see citing works
Brown, S., Martinez, M. J., & Parsons, L. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04785.x · Cited by 371 · see citing works
fMRI reveals two distinct cerebral networks subserving speech motor control
Riecker, A., Mathiak, K., Wildgruber, D., Erb, M., Hertrich, I., Grodd, W., & Ackermann, H. (2005) · Neurology · doi:10.1212/01.wnl.0000152156.90779.89 · Cited by 327 · see citing works
Shared and distinct neural correlates of singing and speaking
ozdemir, E., Norton, A. C., & Gottfried Schlaug, A. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.07.013 · Cited by 325 · see citing works
Riecker, A., Ackermann, H., Wildgruber, D., Dogil, G., & Grodd, W. (2000) · Neuroreport · doi:10.1097/00001756-200006260-00038 · Cited by 318 · see citing works
Speech Science Primer: Physiology, Acoustics, and Perception of Speech
Raphael, L. J., Borden, G. J., & Harris, K. S. (1980) · Medical Entomology and Zoology · Cited by 295 · see citing works
Neural correlates of voluntary breathing in humans
McKay, L. C., Evans, K. C., Frackowiak, R. S. J., & Corfield, D. R. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00641.2002 · Cited by 276 · see citing works
Nielsen, J. M. (1960) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(60)90092-4 · Cited by 249 · see citing works
Regional cerebral blood flow during volitional breathing in man.
Colebatch, J. G., Adams, L. M., Murphy, K., Martin, A. J., Lammertsma, A. A., Tochon‐Danguy, H., Clark, J. C., Friston, K. J., & Guz, A. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018824 · Cited by 219 · see citing works
Comparing cortical activations for silent and overt speech using event-related fMRI
Huang, J., Carr, T. H., & Cao, Y. (2002) · Human Brain Mapping · doi:10.1002/hbm.1060 · Cited by 216 · see citing works
Wildgruber, D., Ackermann, H., & Grodd, W. (2001) · NeuroImage · doi:10.1006/nimg.2000.0672 · Cited by 206 · see citing works
The song system of the human brain
Brown, S., Martinez, M. J., Hodges, D. A., Fox, P. T., & Parsons, L. M. (2004) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2004.03.016 · Cited by 189 · see citing works
Words in melody: an H215O PET study of brain activation during singing and speaking
Jeffries, K. J., Fritz, J. B., & Braun, A. (2003) · Neuroreport · doi:10.1097/00001756-200304150-00018 · Cited by 180 · see citing works
Functional lateralization of speech production at primary motor cortex: a fMRI study
Wildgruber, D., Ackermann, H., Klose, U., Kardatzki, B., & Grodd, W. (1996) · Neuroreport · doi:10.1097/00001756-199611040-00077 · Cited by 175 · see citing works
Localization of cerebral activity during simple singing
Perry, D. W., Zatorre, R. J., Petrides, M., Alivisatos, B., Meyer, E., & Evans, A. C. (1999) · Neuroreport · doi:10.1097/00001756-199911080-00035 · Cited by 166 · see citing works
Ramsay, S. C., Adams, L., Murphy, K., Corfield, D. R., Grootoonk, S., Bailey, D. L., Frackowiak, R. S., & Guz, A. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019503 · Cited by 162 · see citing works
Bayesian inference applied to the electromagnetic inverse problem
Schmidt, D. M., George, J. S., & Wood, C. C. (1999) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(1999)7:3 · Cited by 159 · see citing works
Cortical lesion effects and vocalization in the squirrel monkey
Kirzinger, A., & Jürgens, U. (1982) · Brain Research · doi:10.1016/0006-8993(82)91204-5 · Cited by 157 · see citing works
Functional Neuroanatomy of Human Vocalization: An H215O PET Study
Schulz, G. M., Varga, M., Jeffires, K., Ludlow, C. L., & Braun, A. R. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi061 · Cited by 156 · see citing works
Self-citationExperimental designs and processing strategies for fMRI studies involving overt verbal responses
Birn, R. M., Cox, R. W., & Bandettini, P. A. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.039 · Cited by 154 · see citing works
Evans, K. C., Shea, S. A., & Saykin, A. J. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00383.x · Cited by 153 · see citing works
Cerebral areas associated with motor control of speech in humans
Murphy, K., Corfield, D. R., Guz, A., Fink, G. R., Wise, R. J. S., Harrison, J., & Adams, L. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.83.5.1438 · Cited by 149 · see citing works
Evidence for limbic system activation during CO2‐stimulated breathing in man.
Corfield, D. R., Fink, G. R., Ramsay, S. C., Murphy, K., Harty, H. R., Watson, J. D. G., Adams, L. M., Frackowiak, R. S. J., & Guz, A. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020947 · Cited by 144 · see citing works
Localization of cerebral activity during simple singing
Perry, D. W., Zatorre, R. J., Petrides, M., Alivisatos, B., Meyer, E., & Evans, A. C. (1999) · Neuroreport · doi:10.1097/00001756-199912160-00046 · Cited by 133 · see citing works
Neural control of vocalization: Respiratory and emotional influences
Davis, P. J., Zhang, S., Winkworth, A. L., & Bandler, R. J. (1996) · Journal of Voice · doi:10.1016/s0892-1997(96)80016-6 · Cited by 125 · see citing works
“Silent event-related” fMRI reveals reduced sensorimotor activation in laryngeal dystonia
Haslinger, B. A., Erhard, P., Dresel, C., Castrop, F., Röttinger, M., & Ceballos-Baumann, A. (2005) · Neurology · doi:10.1212/01.wnl.0000184478.59063.db · Cited by 124 · see citing works
Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey.
Simonyan, K., & Jürgens, U. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02548-4 · Cited by 123 · see citing works
Self-citationThe contribution of the cerebellum to speech processing
Ackermann, H., & Hertrich, I. (2000) · Journal of Neurolinguistics · doi:10.1016/s0911-6044(00)00006-3 · Cited by 107 · see citing works
Early pitch-shift response is active in both steady and dynamic voice pitch control
Burnett, T. A., & Larson, C. R. (2002) · The Journal of the Acoustical Society of America · doi:10.1121/1.1487844 · Cited by 99 · see citing works
Effects of Levodopa on Laryngeal Muscle Activity for Voice Onset and Offset in Parkinson Disease
Gallena, S. K., Smith, P. J., Zeffiro, T. A., & Ludlow, C. L. (2001) · Journal of Speech Language and Hearing Research · doi:10.1044/1092-4388(2001/100 · Cited by 88 · see citing works
Self-citationTremblay, P., & Gracco, V. L. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.07.041 · Cited by 87 · see citing works
Speech Science Primer: Physiology, Acoustics, and Perception of Speech
Bailey, B. J. (1981) · Archives of Otolaryngology - Head and Neck Surgery · doi:10.1001/archotol.1981.00790380061018 · Cited by 83 · see citing works
Are Brain Functions Really Additive?
Sidtis, J. J., Strother, S. C., Anderson, J. R., & Rottenberg, D. A. (1999) · NeuroImage · doi:10.1006/nimg.1999.0423 · Cited by 69 · see citing works
Finnegan, E. M., Luschei, E. S., & Hoffman, H. T. (2000) · Journal of Speech Language and Hearing Research · doi:10.1044/jslhr.4304.934 · Cited by 68 · see citing works
Poletto, C. J., Verdun, L., Strominger, R. N., & Ludlow, C. (2004) · Journal of applied physiology · doi:10.1152/japplphysiol.00087.2004 · Cited by 67 · see citing works
Self-citationCortico-cortical projections of the motorcortical larynx area in the rhesus monkey
Simonyan, K., & Jürgens, U. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02960-8 · Cited by 64 · see citing works
Self-citationThe functional neuroanatomy of coordinated orofacial movements: sparse sampling fMRI of whistling
Dresel, C., Castrop, F., Haslinger, B., Wohlschlaeger, A. M., Hennenlotter, A., & Ceballos-Baumann, A. O. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.021 · Cited by 63 · see citing works
The role of the anterior cingulate cortex in pitch variation during sad affect
Barrett, J., Pike, G. B., & Paus, T. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03113.x · Cited by 37 · see citing works
Langers, D. R. M., van Dijk, P., & Backes, W. H. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20315 · Cited by 36 · see citing works
Schaufelberger, M. S., Senhorini, M. C. T., Barreiros, M. Â. M., et al. (2005) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462005000300013 · Cited by 34 · see citing works
Laryngeal muscles and articulatory control
Löfqvist, A., McGarr, N. S., & Honda, K. (1984) · The Journal of the Acoustical Society of America · doi:10.1121/1.391278 · Cited by 24 · see citing works
Cortical activities relating to modulation of sound frequency: how to vocalize?
Gunji, A., Kakigi, R., & Hoshiyama, M. (2003) · Cognitive Brain Research · doi:10.1016/s0926-6410(03)00165-4 · Cited by 7 · see citing works
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Herrero, J. L., Khuvis, S., Yeagle, E., Cerf, M., & Mehta, A. D. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00551.2017 · Cited by 338 · see citing works
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- Authors
- Loucks, T. M. J., Poletto, C. J., Simonyan, K., Reynolds, C. L., & Ludlow, C. L.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Ludlow, Christy L.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2007-05
- Volume
- 36
- Issue
- 1
- Pages
- 131-143
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC1959512
- OpenAlex
- W2143096004
- Cited by
- 150
- References
- 55
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 7 · 2021: 21 · 2020: 11 · 2019: 4 · 2018: 5 · 2017: 10 · 2016: 10 · 2015: 8 · 2014: 10 · 2013: 2 · 2012: 9
- FWCI
- 3.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (Z01NS002980)
- NHLBI Division of Intramural Research
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Phonetics and Phonology Research
- Health Sciences › Medicine › Physiology › Voice and Speech Disorders
- Keywords
- phonation, exhalation, speech production, laryngeal control, respiratory control, upper airway, volitional control, auditory cortex, sensorimotor cortex, temporoparietal cortex, dentate nucleus, cerebellum, glottal stop, vowel production, neural coordination
- MeSH terms
- Adult, Aged, Attention, Brain, Brain Mapping, Cerebral Cortex, Female, Glottis, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Oxygen, Phonation, Speech, Vocal Cords, Exhalation
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