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01-01-2014 | Research Article

Voice-related modulation of mechanosensory detection thresholds in the human larynx

Authors: Michael J. Hammer, Mallory A. Krueger

Published in: Experimental Brain Research | Issue 1/2014

Abstract

Rapidly adapting mechanoreceptors within the laryngeal mucosa provide the central nervous system with perceptual and proprioceptive afference for a variety of essential yet diverse human functions including voice sound production and airway protection. It is unknown why mechanosensory information that yields a defensive response when an individual breathes may go largely unnoticed when the individual voices. Therefore, a central question is whether there is voice-related modulation of laryngeal mechanosensory detection. Such modulation would be consistent with current models of afferent laryngeal control, and may be important to maintain fluent voice in the presence of potentially distracting sensory input. Therefore, we employed endoscopic assessment of laryngeal mechanosensory detection thresholds in ten healthy adults during tidal breathing and a voice task. We tested the hypothesis that laryngeal mechanosensory detection thresholds would be higher during the voice task. We found that thresholds were significantly higher for all participants during the voice task and that these changes were significantly more modest in women. Our findings suggest that the laryngeal sensorium may modulate mechanosensory afference to attenuate the potentially distracting influence of sensory input during voice. The finding that women maintain a greater sensitivity during the voice task than men (lower thresholds) may have important implications for the higher prevalence of sensorimotor voice disturbances in women. Our results are consistent with the presence of mechanosensory modulation in other motor systems and with observed sensory differences between women and men. Such modulation has important implications for understanding the underlying neural mechanisms of laryngeal control and how these mechanisms may operate in individuals with laryngeal disturbances.

Andreatta RD, Barlow SM (2003) Movement-related modulation of vibrotactile detection thresholds in the human orofacial system. Exp Brain Res 149:75–82PubMed

Andreatta RD, Mann EA, Poletto CJ, Ludlow CL (2002) Mucosal afferents mediate laryngeal adductor responses in the cat. J Appl Physiol 93:1622–1629PubMed

Bajaj P, Arendt-Nielsen L, Bajaj P, Madsen H (2001) Sensory changes during the ovulatory phase of the menstrual cycle in healthy women. Eur J Pain 5:135–144PubMedCrossRef

Behroozmand R, Larson CR (2011) Error-dependent modulation of speech-induced auditory suppression for pitch-shifted voice feedback. BMC Neurosci 12:54PubMedCentralPubMedCrossRef

Behroozmand R, Karvelis L, Liu H, Larson CR (2009) Vocalization-induced enhancement of the auditory cortex responsiveness during voice F0 feedback perturbation. Clin Neurophysiol 120:1303–1312PubMedCentralPubMedCrossRef

Bevan L, Cordo P, Carlton L, Carlton M (1994) Proprioceptive coordination of movement sequences: discrimination of joint angle versus angular distance. J Neurophysiol 71:1862–1872PubMed

Chen Z, Liu P, Jones JA, Huang D, Liu H (2010) Sex-related differences in vocal responses to pitch feedback perturbations during sustained vocalization. J Acoust Soc Am 128:EL355–EL360PubMed

Chesterton LS, Barlas P, Foster NE, Baxter GD, Wright CC (2003) Gender differences in pressure pain threshold in healthy humans. Pain 101:259–266PubMedCrossRef

Chiao GZ, Larson CR, Yajima Y, Ko P, Kahrilas PJ (1994) Neuronal activity in nucleus ambiguous during deglutition and vocalization in conscious monkeys. Exp Brain Res 100:29–38PubMedCrossRef

Cordo P, Carlton L, Bevan L, Carlton M, Kerr GK (1994) Proprioceptive coordination of movement sequences: role of velocity and position information. J Neurophysiol 71:1848–1861PubMed

Davis PJ, Zhang SP, Bandler R (1996) Midbrain and medullary regulation of respiration and vocalization. Prog Brain Res 107:315–325PubMedCrossRef

Dicpinigaitis PV, Rauf K (1998) The influence of gender on cough reflex sensitivity. Chest 113:1319–1321PubMedCrossRef

Dicpinigaitis PV, Allusson VR, Baldanti A, Nalamati JR (2001) Ethnic and gender differences in cough reflex sensitivity. Respiration 68:480–482PubMedCrossRef

Edin BB (1992) Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J Neurophysiol 67:1105–1113PubMed

Edin BB (2004) Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. J Neurophysiol 92:3233–3243PubMedCrossRef

Edin BB, Johansson N (1995) Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol 487:243–251PubMed

Feine JS, Chapman CE, Lund JP, Duncan GH, Bushnell MC (1990) The perception of painful and nonpainful stimuli during voluntary motor activity in man. Somatosens Mot Res 7:113–124PubMedCrossRef

Fillingim RB, Ness TJ (2000) Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev 24:485–501PubMedCrossRef

Gui P, Ebihara S, Kanezaki M, Suda C, Nikkuni E, Ebihara T, Yamasaki M, Kohzuki M (2010) Gender differences in perceptions of urge to cough and dyspnea induced by citric acid in healthy never smokers. Chest 138:1166–1172PubMedCrossRef

Hammer MJ (2009) Design of a new somatosensory stimulus delivery device for measuring laryngeal mechanosensory detection thresholds in humans. IEEE Trans Biomed Eng 56:1154–1159PubMedCentralPubMedCrossRef

Hammer MJ, Barlow SM (2010) Laryngeal somatosensory deficits in Parkinson’s disease: implications for speech respiratory and phonatory control. Exp Brain Res 201:401–409PubMedCentralPubMedCrossRef

Hammer MJ, Murpy CA, Abrams TM (2013) Airway somatosensory deficits and dysphagia in Parkinson’s disease. J Parkinsons Dis 3:39–44PubMedCentralPubMed

Harju EL (2002) Cold and warmth perception mapped for age, gender, and body area. Somatosens Mot Res 19:61–75PubMedCrossRef

Hetrick WP, Sandman CA, Bunney WE Jr, Jin Y, Potkin SG, White MH (1996) Gender differences in gating of the auditory evoked potential in normal subjects. Biol Psychiatry 39:51–58PubMedCrossRef

Hunter EJ, Tanner K, Smith ME (2011) Gender differences affecting vocal health of women in vocally demanding careers. Logoped Phoniatr Vocol 36:128–136PubMedCentralPubMedCrossRef

Ide A, Aboitiz F (2001) A sex difference in the postcentral sulcus of the human brain. Brain Res 890:330–332PubMedCrossRef

Jurgens U (2002) Neural pathways underlying vocal control. Neurosci Biobehav Rev 26:235–258PubMedCrossRef

Jurgens U, Kirzinger A (1985) The laryngeal sensory pathway and its role in phonation. A brain lesioning study in the squirrel monkey. Exp Brain Res 59:118–124PubMedCrossRef

Kelsall A, Decalmer S, McGuinness K, Woodcock A, Smith JA (2009) Sex differences and predictors of objective cough frequency in chronic cough. Thorax 64:393–398PubMedCrossRef

Kirchner JA, Wyke BD (1965) Articular reflex mechanisms in the larynx. Ann Otol Rhinol Laryngol 74:749–768PubMed

Kogo M, Iida S, Senoo H, Ishii S, Hamaguchi M, Enomoto A, Matsuya T (2003) Effects of subglottal air pressure on velopharyngeal muscle activity in dogs. Cleft Palate Craniofac J 40:351–355PubMedCrossRef

Larson CR (1991) On the relation of PAG neurons to laryngeal and respiratory muscles during vocalization in the monkey. Brain Res 552(1):77–86PubMedCrossRef

Larson CR, Yajima Y, Ko P (1994) Modification in activity of medullary respiratory-related neurons for vocalization and swallowing. J Neurophysiol 71:2294–2304PubMed

Larson CR, Altman KW, Liu H, Hain TC (2008) Interactions between auditory and somatosensory feedback for voice F0 control. Exp Brain Res 187:613–621PubMedCentralPubMedCrossRef

Linnman C, Beucke JC, Jensen KB, Gollub RL, Kong J (2012) Sex similarities and differences in pain-related periaqueductal gray connectivity. Pain 153:444–454PubMedCentralPubMedCrossRef

Liu H, Behroozmand R, Larson CR (2010) Audio–vocal interactions in the mammalian brain. In: Brudzynski SM (ed) Handbook of mammalian vocalization: an integrative neuroscience approach. Academic Press, San Diego, pp 393–401CrossRef

Liu H, Meshman M, Behroozmand R, Larson CR (2011) Differential effects of perturbation direction and magnitude on the neural processing of voice pitch feedback. Clin Neurophysiol 122:951–957PubMedCentralPubMedCrossRef

Loucks TM, Poletto CJ, Saxon KG, Ludlow CL (2005) Laryngeal muscle responses to mechanical displacement of the thyroid cartilage in humans. J Appl Physiol 99:922–930PubMedCentralPubMedCrossRef

Malannino N (1974) Proceedings: laryngeal neuromuscular spindles and their possible function. Folia Phoniatr 26:291–292CrossRef

Matos R, Wang K, Jensen JD, Jensen T, Neuman B, Svensson P, Arendt-Nielsen L (2011) Quantitative sensory testing in the trigeminal region: site and gender differences. J Orofac Pain 25:161–169PubMed

Matsuo H, Shin T (1994) Distribution of intraepithelial nerve fibers in the feline glottis. Otolaryngol Head Neck Surg 111:91–99PubMed

Nishino T (2011) Dyspnoea: underlying mechanisms and treatment. Br J Anaesth 106:463–474PubMedCrossRef

Nishino T, Isono S, Ishikawa T, Shinozuka N (2008) Sex differences in the effect of dyspnea on thermal pain threshold in young healthy subjects. Anesthesiology 109:1100–1106PubMedCrossRef

Parkinson AL, Flagmeier SG, Manes JL, Larson CR, Rogers B, Robin DA (2012) Understanding the neural mechanisms involved in sensory control of voice production. NeuroImage 61:314–322PubMedCentralPubMedCrossRef

Patterson JV, Hetrick WP, Boutros NN, Jin Y, Sandman C, Stern H, Potkin S, Bunney WE Jr (2008) P50 sensory gating ratios in schizophrenics and controls: a review and data analysis. Psychiatry Res 158:226–247PubMedCrossRef

Peters RM, Hackeman E, Goldreich D (2009) Diminutive digits discern delicate details: fingertip size and the sex difference in tactile spatial acuity. J Neurosci 29:15756–15761PubMedCrossRef

Post LJ, Zompa IC, Chapman CE (1994) Perception of vibrotactile stimuli during motor activity in human subjects. Exp Brain Res 100:107–120PubMedCrossRef

Roy N, Merrill RM, Gray SD, Smith EM (2005) Voice disorders in the general population: prevalence, risk factors, and occupational impact. Laryngoscope 115:1988–1995PubMedCrossRef

Sampson S, Eyzaguirre C (1964) Some functional characteristics of mechanoreceptors in the larynx of the cat. J Neurophysiol 27:464–480PubMed

Sant’Ambrogio G, Mathew OP (1986) Laryngeal receptors and their reflex responses. Clin Chest Med 7:211–222PubMed

Sapir S, Baker KK, Larson CR, Ramig LO (2000) Short-latency changes in voice F0 and neck surface EMG induced by mechanical perturbations of the larynx during sustained vowel phonation. J Speech Lang Hear Res 43(1):268–276PubMed

Schmidt RF, Schady WJ, Torebjork HE (1990) Gating of tactile input from the hand. I. Effects of finger movement. Exp Brain Res 79:97–102PubMedCrossRef

Shiba K, Yoshida K, Nakajima Y, Konno A (1997) Influences of laryngeal afferent inputs on intralaryngeal muscle activity during vocalization in the cat. Neurosci Res 27:85–92PubMedCrossRef

Shiba K, Miura T, Yuza J, Sakamoto T, Nakajima Y (1999) Laryngeal afferent inputs during vocalization in the cat. Neuroreport 10:987–991PubMedCrossRef

Simonyan K, Jurgens U (2005a) Afferent cortical connections of the motor cortical larynx area in the rhesus monkey. Neuroscience 130:133–149PubMedCrossRef

Simonyan K, Jurgens U (2005b) Afferent subcortical connections into the motor cortical larynx area in the rhesus monkey. Neuroscience 130:119–131PubMedCrossRef

Smith E, Kirchner HL, Taylor M, Hoffman H, Lemke JH (1998) Voice problems among teachers: differences by gender and teaching characteristics. J Voice 12:328–334PubMedCrossRef

Titze IR (1989) Physiologic and acoustic differences between male and female voices. J Acoust Soc Am 85:1699–1707PubMedCrossRef

Titze IR (1994) Principles of voice production. Allyn & Bacon Inc., Boston

Titze IR, Finnegan EM, Laukkanen AM, Fuja M, Hoffman H (2008) Laryngeal muscle activity in giggle: a damped oscillation model. J Voice 22:644–648PubMedCrossRef

Tomasi D, Chang L, Caparelli EC, Ernst T (2008) Sex differences in sensory gating of the thalamus during auditory interference of visual attention tasks. Neuroscience 151:1006–1015PubMedCentralPubMedCrossRef

Yoshida Y, Tanaka Y, Hirano M, Nakashima T (2000) Sensory innervation of the pharynx and larynx. Am J Med 108(Suppl 4a):51S–61SPubMedCrossRef

Title: Voice-related modulation of mechanosensory detection thresholds in the human larynx
Authors: Michael J. Hammer
Mallory A. Krueger
Publication date: 01-01-2014
Publisher: Springer Berlin Heidelberg
Published in: Experimental Brain Research / Issue 1/2014
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-013-3703-1

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Voice-related modulation of mechanosensory detection thresholds in the human larynx

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