Abstract
Sensitivity of vestibular system to sounds (SVSS) can be measureable by cervical vestibular evoked myogenic potentials (cVEMPs). The aim of this study is to investigate central representation of vestibular system sensitivity to sound. The research was conducted in 2022–2023 by searching English language databases. The criterion for selecting documents was their overlap with the aim of this work. The animals studies were not included. The saccule is stimulated by sounds, that are transmitted through air and bone conduction. Utricle and semicircular canals are activated only by the vibrations. The afferent nerve fibers of the vestibular system project to the temporal, frontal, parietal, primary visual cortex, insula and the cingulate cortex. There is a relationship between normal results of the cVEMPs and these parameters. Improved phonemes recognition scores and word recognition scores in white noise, the efficiency of auditory training, incraed amplitude of the auditory brainstem responses to 500 HZ tone burst. Learning the first words is not only based on the hearing and other senses participate. The auditory object is a three-dimensional imaging in people's minds, when they hear a word. The words expressed by a speaker create different auditory objects in people's minds. Each of these auditory objects has its own color, shape, aroma and characteristics. For the formation of the auditory objects, all senses and whole areas of the brain contribute. Like other senses, central representation of vestibular system sensitivity to sound are also involved in the formation of auditory objects.
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Introduction
The human inner ear is consisted of two separate organs; the cochlea and vestibule. The cochlea is an organ of hearing, the vestibule is responsible for maintaining the body's balance in linear and angular accelerations [1, 2]. The SVSS in human has been confirmed by invention of the cVEMPs [3,4,5,6,7,8,9]. It is generated during the stimulation of the sternocleidomastoid muscle with intense low frequency sounds [3, 10, 11]. The saccule has highest sound sensitivity between vestibular organs [12,13,14].
Pathologies that involve the inner ear cochlea, also cause damage to the saccule. Then, the most susceptibility of the vestibular organs to impairment is related to the saccule, in cases of sensorineural hearing loss [15, 16], Meniere's disease [17], sudden sensorineural hearing loss [18, 19], auditory-neuropathy [20], noise induced hearing loss [21], destructive effects of musical sounds [22], aging [23], ototoxic drugs [24], and covid-19 [25]. Also, continuous loudly singing, which lasts longer than duration time of the stapedius reflex of the middle ear can cause saccular damage [26]. In addition, the recovery of the patients with acute low-frequency sensorineural hearing loss and saccular damage is weaker than similar cases with normal saccular function [27].
The most important reason for saccular susceptibility to impairment is the proximity of the saccule to the cochlea through the Reunion duct [2], which connects the lower part of the saccule to the cochlear duct near its vestibular extremity [1].
The aim of this study is to investigate central representation of vestibular system sensitivity to sound. In order to retrieve original documents that were published between 2000 and 2022, information sources about SVSS in human were studied, such as Science Citation Index, Web of Science, PubMed, PubMed/Medline, Scopus, Springer, Pearson, Google Scholar. First, 89 documents were found, and finally 58 papers that were related to the title of this study were considered. The criterion for selecting articles was their overlap with the purpose of this work and gain access to the full text of the sources. The SVSS in animal literatures was not included.
Results
A summary of the conclusion section of the published articles on sensitivity of vestibular system to sounds in the years 2000 to 2023 is presented in Table 1.
Discussion
Based on the findings reported in the results section of this research, the human vestibular system is sound sensitive and sends signals to the neural centers of the brainstem and the brain. Now, this question is raised: Are the neural information from the vestibular system useful in the neural processing? To answer this question, it is necessary to take a brief look at how to learn new words.
Learning the first language for every native listener is a natural part of that person's daily life, which is formed based on the relationship he/she has with the world around him. The first language of a child is part of that child's personal, social and cultural identity, it brings about the reflection and learning of effective social patterns of acting and speaking [48]. To perception the world, contribution of all senses is necessary. Learning the first words is not only based on the hearing and other senses participate. The auditory object is a three-dimensional imaging in people's minds, when they hear a word. The words expressed by a speaker create different auditory Objects in people's minds. For example, upon hearing the word "flower", different auditory objects of flower may be represented for people; a flower in a glass, a flower in a garden, a faded flower, a flower in a bride's hand or a flower on a tombstone. Each of these auditory objects has its own color, shape, aroma and characteristics. Then for a native listener, each spoken word is equivalent to an auditory object. For the formation of the auditory objects, all senses and whole areas of the brain contribute [49].
Speech-in-noise perception is also done with the participation of all areas of the brain. The neural centers for speech perception are various and temporal lobe is influenced by several sensory processings and mechanisms, the auditory brain is not actually monosensory and had multi-modal processing [38, 50, 51].
The vision also plays a guiding role in the formation and maturation of auditory responses. If the visual signals are damaged during childhood, the auditory representation in the superior colliculus is impaired due to the disturbance in the normal development. Vision problems due to surgery or head trauma can disturb the auditory spatial balance in the nucleus of the superior colliculus [52].
The inferior frontal gyrus improves people’s accuracy in repeating unfamiliar foreign speech sounds, and matches perceived speech to produced speech [49]. Mirror-neuron brain areas, which have no role in interpretation of high-level activities and are involved in low-level processing have a precise and essential role in speech-in-noise perception [53].
The insula in the left cortex is exactly motivated when main frequency of human voices transport lexical information to a native listener, whereas the insula of the right cortex is activated once main frequency of human voices do not provide lexical information [48]. The cingulo-opercular system is involved in central-peripheral processing of attention and control [49]. Therefore, the neural signals from the vestibular system project to various areas of the brain and participate to other senses for formation the auditory Objects.
The SVSS is in the range of the fundamental frequency of the human voice [36], which differs between men = 100HZ, women = 200HZ, and infants = up to 400HZ [54]. Considering that the saccule is close to the larynx and is also connected to the cochlea [2], the afferent nerve fibers of the saccule are stimulated during self-voice production [34, 38], and the person ossifies his own voice through feedback control or bone-conducted pathway [38].
Saccular nerve fibers spirit to the brainstem. The brainstem is also sensitive to low-frequency sounds and participates in detection the pitch of speech and the melody of music. The brainstem encodes the first formant of speech (the lowest frequency or the strongest harmonic of the speaker's voice), which is necessary for the perception of vowels [51, 54]. Therefore, the acoustical information of the vestibular system that goes to the brainstem may be effective in detection beats and pitch [30, 33].
The SVSS can be motivated when people participate in group activities in noisy competing situations, e.g. singing poetry together, chanting in the crowd, shouting in the group, cheering on their favorite team in sports activities, performing military parades, and similar cases [7, 9, 38, 39, 55,56,57,58].
The limbic receives inputs from vestibular afferent nerve fibers and regulates emotions, such as anger, joy, hate, sadness [28]. The limbic is also connected to musculo-skeletal systems [8, 9]. Then, intense low-frequency sounds stimulate the saccule, the limbic, the musculo-skeletal systems [9] and generate the desire to perform the harmonic movements, in the form of pacing, marching, clapping or chest beating [28, 31, 41].
Conclusion
For the formation of the auditory objects, all senses and whole areas of the brain contribute. Like other senses, central representation of vestibular system sensitivity to sound are also involved in the formation of auditory objects.
Abbreviations
- cVEMPs:
-
Vestibular evoked myogenic potentials
- SVSS:
-
Sensitivity of vestibular system to sounds
References
Murofushi TKK (2009) Sound sensitivity of the vestibular end-organs and sound-evoked vestibule collic reflexes in mammals. In: Murofushi T KK, Kaga K. (eds), Issues in Vestibular Evoked Myogenic Potential. E-Publishing Springer Press Nikkei Printing, Japan. Inc. pp 20–25
Eatock RA, Lysakowski A (2006) Mammalian Vestibular Hair Cells. In: Eatock RA, Fay RR, Popper AN (eds) Vertebrate Hair Cells. Handbook of Auditory research, Publishing Springer, New York, 8, pp 349
Colebatch JG (2006) Assessing saccular (otolith) function in man. Acoust Soc Am 119(5):3432. https://doi.org/10.1121/1.4786895
Lenhardt ML (2006) Saccular hearing; turtle model for a human prosthesis. Acoust Soc Am 119(5):3433. https://doi.org/10.1121/1.4786900
Sheykholeslami K, Schmerber S, Kermany MH (2004) Vestibular-evoked myogenic potentials in three patients with large vestibular aqueduct. Hear Res 190:161–216. https://doi.org/10.1016/S0378-5955(04)00018-8
Sheykholeslami K, Habiby M, Kermany MH, Kaga K (2001) Frequency sensitivity range of the saccule to bone-conducted stimuli measured by vestibular evoked myogenic potentials. Hear Res 160(1–2):58–62. https://doi.org/10.1016/s0378-5955(01)00333-1
Sheykholeslami K, Kaga K (2002) The otolithic organ as a receptor of vestibular hearing revealed by vestibular-evoked myogenic potentials in patients with inner ear anomalie. Hear Res 165:62–67. https://doi.org/10.1016/s0378-5955(02)00278-2
Todd NPM (2001) Evidence for a behavioral significance of saccular acoustic sensitivity in humans. Acoust Soc Am 110(1):380–390. https://doi.org/10.1121/1.1373662
Todd NPM, Frederick WCJ, Banks JR (2000) Saccular origin of frequency tuning in myogenic vestibular evoked potentials? IMPLICATIONS for human responses to loud sounds. Hear Res. https://doi.org/10.1016/s0378-5955(99)00222-1
Curthoys IS, Vulovic V, Burgess AM, Cornell ED, Mezey LE, Macdougall HG (2011) The basis for using bone-conducted vibration or air-conducted sound to test otolithic function. Ann N Y Acad Sci 146(2):274–280. https://doi.org/10.3389/fneur.2018.00366
Welgampola MS, Rosengren SM, Halmagyi GM, Colebatch JG (2003) Vestibular activation by bone conducted sound. Neurol Neurosurg Psychiatry 74:771–778. https://doi.org/10.1136/jnnp.74.6.771
Oh SY, Boegle R, Ertl M, Stephan T, Dieterich M (2018) Multisensory vestibular, vestibular-auditory, and auditory network effects revealed by parametric sound pressure stimulation. Neuroimage 1(176):354–363. https://doi.org/10.1016/j.Neuroimage.2018.04.057
Longridge NS, Lim A, Mallinson AI, Renshaw J (2020) Vestibular suppression of normal bodily sounds. Acta Otolaryngol 140(5):401–405. https://doi.org/10.1080/00016489.2020.1723807. (Epub 2020 Feb 18)
Fröhlich L, Wilke M, Plontke SK, Rahne T (2021) Bone conducted vibration is an effective stimulus for otolith testing in cochlear implant patients. Vestibular research 32(4):355–365. https://doi.org/10.3233/VES-210028
Sazgar AA, Dortaj V, Akrami K, Akrami S, Karimi Yazdi AR (2006) Saccular damage in patients with high-frequency sensorineural hearing loss. Eur Arch Otorhinolaryngol 263(7):608–613. https://doi.org/10.1007/s00405-006-0038-6
Tian L et al (2022) High frequency hearing loss may act as a screening index evaluating otolith function in vertigo patients with normal semi-circular canal function. Front Neurol 13:978490. https://doi.org/10.3389/fneur.2022.978490
Guajardo-Vergara C et al (2022) Endolymphatic hydrops in the unaffected ear of patients with unilateral Ménière’s disease. Eur Arch Otorhinolaryngol 279(12):5591–5600. https://doi.org/10.1007/s00405-022-07412-9
Jiang Z et al (2021) Contribution of audiogram classification in evaluating vestibular dysfunction in sudden sensorineural hearing loss with vertigo. Front Neurol 12:667804. https://doi.org/10.3389/fneur.2021.667804
Hong SM, Byun JY, Park CH, Lee JH, Park MS, Cha CI (2008) Saccular damage in patients with idiopathic sudden sensorineural hearing loss without vertigo. Otolaryngol Head Neck Surg 139(4):541–545. https://doi.org/10.1016/j.otohns.2008.07.003
Emami SF, Farahani F (2015) Saccular dysfunction in children with sensorineural hearing loss and auditory neuropathy/auditory dys-synchrony. Acta Otolaryngol 135(12):1298–1303. https://doi.org/10.3109/00016489.2015.1076169
Stewart CE (2020) Effects of noise exposure on the vestibular system: a systematic review. Front Neurol. https://doi.org/10.3389/fneur.2020.593919
Emami SF (2014) Acoustic sensitivity of the saccule and daf music. Iranian J Otorhinolaryngol 26(75):105 (PMID: 24744999)
Emami SF, Abdoli A (2015) Saccular dysfunction in low-frequency age-related sensorineural hearing loss. Otolaryngol Open Access J. https://doi.org/10.23880/ooaj-16000151
Huang Y, Mao H, Chen Y (2022) Regeneration of hair cells in the human vestibular system. Front Mol Neurosci 15:854635. https://doi.org/10.3389/fnmol.854635
Aydin S et al (2022) The effect of the severity of COVID-19 on the sequelae of the audiovestibular system. Ear Nose Throat. https://doi.org/10.1177/01455613221083826
Emami SF (2016) The effect of loud human’s voice on saccular function. J Int Res Med Pharm Sci 7(4):153–158
Wang C-T, Min FK, Yi-Ho Y, Wen CP (2010) Vestibular-evoked myogenic potential in the prediction of recovery from acute low-tone sensorineural hearing loss. Ear Hear 31(2):289–295. https://doi.org/10.1097/AUD.0b013e3181c5b743
Todd NPM, Cody FW (2000) Vestibular responses to loud dance music: a physiological basis of the rock and roll threshold? Acoust Soc Am 107(1):496–500. https://doi.org/10.1121/1.428317
Todd NPM, Rosengren SM, Colebatch JG (2009) A utricular origin of frequency tuning to low-frequency vibration in the human vestibular system? Neurosci Lett 451:175–180. https://doi.org/10.1016/j.neulet.2008.12.055
Emami SF, Daneshi A (2012) Vestibular hearing and neural synchronization. ISRN Otolaryngol. https://doi.org/10.5402/2012/246065
Butler B, Trainor L (2015) The musician redefined: a behavioral assessment of rhythm perception in professional club DJs. Timing Time Percept 3(1–2):116–132. https://doi.org/10.1163/22134468-03002041
Kassow MS, Wilkinson D, Denby E, Ferguson H (2016) Synchronised vestibular signals increase the P300 event-related potential elicited by auditory oddballs. Brain Res 1648:224–231. https://doi.org/10.1016/j.brainres.2016.07.019
Emami SF, Gohary N (2014) The vestibular-auditory interaction for auditory brainstem response to low frequencies. ISRN Otolaryngol. https://doi.org/10.1155/2014/103598
Trivelli M, Potena M, Frari V, Petitti T, Deidda V, Salvinelli F (2013) Compensatory role of saccule in deaf children and adults: novel hypotheses. Med Hypotheses 80(1):43–46. https://doi.org/10.1016/j.mehy.2012.10.006
Emami SF (2016) Studying the effect of auditory training on cervical vestibular evoked myogenic potentials in primary school age deaf children. AMUJ 18(10):20–28
Emami SF (2013) Is all human hearing cochlear? Sci World J. https://doi.org/10.1155/2013/147160
Emami SF, Purbakht A, Daneshi A, Sheykholeslami K, Emamjome H, Kammali M (2013) Sound sensitivity of the saccule for low frequencies in healthy adults. ISRN Otolaryngol. https://doi.org/10.1155/2013/429680
Iannotti GR et al (2022) EEG spatiotemporal patterns underlying self-other voice discrimination. Cereb Cortex 32:1978–1992. https://doi.org/10.1093/cercor/bhab329
Emami SF, Purbakht A, Sheykholeslami K, Kammali M, Behnoud F, Daneshi A (2012) Vestibular hearing and speech processing. ISRN Otolaryngol. https://doi.org/10.5402/2012/850629
Emami SF, Nikoo M (2014) Improvement of Stapedial Muscle Reflex Threshold by Acoustic Sensitivity of the Saccule. Sch J App Med Sci 2:3315–3319. https://doi.org/10.36347/sjams.2014.v02i06.091
Phillips-Silver J, Trainor LJ (2008) Vestibular influence on auditory metrical interpretation. Brain Cognit 67(1):94–102. https://doi.org/10.1016/j.bandc.2007.11.007
Todd NPM, Paillard AC, Kluk K, Whittle E, Colebatch JG (2014) Source analysis of short and long latency vestibular-evoked potentials (VsEPs) produced by left vs. right ear air-conducted 500 Hz tone pips. Hear Res 312:91–102. https://doi.org/10.1016/j.heares.2014.03.006
Miyamoto T, Fukushima K, Takada T, Waele CD, Vidal PP (2007) Saccular stimulation of the human cortex: a functional magnetic resonance imaging study. Neurosci Lett 423:68–72. https://doi.org/10.1016/j.neulet.2007.06.036
Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M (2008) Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. Neuroimage 39(1):19–31. https://doi.org/10.1016/j.neuroimage.2007.08.016
McNerney KM, Lockwood AH, Coad ML, Wack DS, Burkard RF (2011) Use of 64-channel electroencephalography to study neural otolith-evoked responses. Am Acad Audiol 22(3):143–155. https://doi.org/10.3766/jaaa.22.3.3
Todd NPM, Paillard AC, Kluk K, Whittle E, Colebatch JG (2013) Vestibular receptors contribute to cortical auditory evoked potentials. Hear Res 309(100):63–74. https://doi.org/10.1016/j.heares.2013.11.008
Emami SF (2014) Hypersensitivity of vestibular system to sound and pseudoconductive hearing loss in deaf patients. ISRN Otolaryngol. https://doi.org/10.1155/2014/817123
Wong PC, Parsons LM, Martinez M, Diehl RL (2004) The role of the insular cortex in pitch pattern perception: the effect of linguistic contexts. Neurosci 24(41):9153–9160. https://doi.org/10.1523/JNEUROSCI.2225-04.2004
Emami SF, Shariatpanahi E (2023) Central representation of speech-in-noise perception: a narrative review. Aud Vestib Res. Article in Press. https://avr.tums.ac.ir/index.php/avr/article/view/1102
Emami SF, Shariatpanahi E, Gohari N, Mehrabifard M (2023) Aging and speech-in-noise perception. Indian J Otolaryngol Head Neck Surg. https://doi.org/10.1007/s12070-023-03689-2
Scott SK, Sinex DG (2010) Speech. In: Rees A, Palmer A (eds) The Oxford handbook of auditory science: the auditory brain, 1st edn. E-Publishing Oxford University Press, New York, pp 193–214
Yonatan IF, Fishman YI, Steinschneider M (2010) Formation of auditory streams. (eds), The Oxford handbook of auditory science: the auditory brain. 1st ed. E-Publishing Oxford university press, New York, pp 215–245
Heyes C, Catmur C (2022) What happened to mirror neurons? Perspect Psychol Sci 17(1):153–168. https://doi.org/10.1177/1745691621990638
Abrams DA, Kraus N (2015) Auditory pathway representations of speech sounds in humans. In: Katz J, Chasin M, English K, Hood LJ, Tillery KL (eds) Hand book of Clinical Audiology, 7th edn. Publishing Wolters Kluwer Health, Philadelphia, pp 527–544
Todd NPM, Govender S, Colebatch JG (2016) Vestibular-dependent inter-stimulus interval effects on sound evoked potentials of central origin. Hear Res 341:190–201. https://doi.org/10.1016/j.heares.2016.07.017
Todd NPM, Lee CS (2015) Source analysis of electrophysiological correlates of beat induction. Front Psych Audit Cogn Neurosci 6:1178. https://doi.org/10.3389/fpsyg.2015.01178
Todd NPM, Rosengren SM, Colebatch JG (2008) Tuning and sensitivity of the human vestibular system to low-frequency vibration. Neurosci Lett. https://doi.org/10.1016/j.neulet.2008b.08.011
Todd NPM, Rosengren SM, Colebatch JG (2003) A short latency vestibular evoked potential produced by bone-conducted acoustic stimulation. Acoust Soc Am 114(6):3264–3272. https://doi.org/10.1121/1.1628249
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Emami, S.F. Central Representation of Cervical Vestibular Evoked Myogenic Potentials. Indian J Otolaryngol Head Neck Surg 75, 2722–2728 (2023). https://doi.org/10.1007/s12070-023-03829-8
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DOI: https://doi.org/10.1007/s12070-023-03829-8