Is all hearing cochlear Karolina Kluk in collaboration

Is all hearing cochlear? Karolina Kluk in collaboration with: Neil Todd Aurore Paillard Elizabeth Whittle James Colebatch BSHAA Congress - Telford 15 th May 2015

Hearing through the vestibular organs In many fish and amphibian species the otolith organs (the saccule and utricle) are important not only for vestibular function but also for detection of sound (Lewis and Narins, 1999) BSHAA Congress - Telford 15 th May 2015

Hearing through the vestibular organs Many fish use vestibularactivating sounds as mating signals. For example male Haddock - a singing fish - vocalizes by drumming on his swim bladder. BSHAA Congress - Telford 15 th May 2015

Hearing through the vestibular organs • Throughout vertebrate evolution, new structures evolved for the detection of sound culminating in the cochlea (Manley et al. , 2004). BSHAA Congress - Telford 15 th May 2015

Hearing through the vestibular organs Hearing through the auditory organ BSHAA Congress - Telford 15 th May 2015

Residual acoustic sensitivity • Acoustic sensitivity of the vestibular organs has been conserved in all classes of vertebrate. (Young et al. , 1977; Mc. Cue and Guinan, 1994; Curthoys et al. , 2006) • However, the predominant view in the field of hearing research is that, whatever the role of the otolith organs in fish and amphibians, residual acoustic sensitivity in mammals is likely to be vestigial and thus not relevant to hearing. BSHAA Congress - Telford 15 th May 2015

Does the vestibular system respond to sound? In humans, acoustic sensitivity of the vestibular organs can be demonstrated by • vestibular-dependent effects like nystagmus (Lackner and Graybiel, 1974) • evoked electromyographic (EMG) signals (Bickford et al. 1964) BSHAA Congress - Telford 15 th May 2015

Vestibular evoked myogenic potentials (VEMP) EMG responses can be measured either from: – muscles of the neck, e. g. the sternocleidomastoid muscle, reflecting the vestibular-collic reflex pathways (the cervical VEMP or c. VEMP) – extra-ocular eye muscles, reflecting activation of the vestibular ocular reflex pathways (ocular VEMP or o. VEMP). BSHAA Congress - Telford 15 th May 2015 c. VEMP o. VEMP

Frequency tuning • The use of VEMPs has enabled considerable advances in our knowledge of the sensitivity of the human otolith organs to sound and vibration. • The two human otolith organs have distinct tuning properties with the saccule tuned to 500 Hz and utricle tuned 100 Hz. BSHAA Congress - Telford 15 th May 2015

VEMP thresholds • For 500 Hz (saccule) air conducted sound activation, vestibular thresholds are at 80 d. B SL (above auditory thresholds) • For 100 Hz (utricle) vibration, vestibular thresholds can be as low as -15 d. B SL (BELOW auditory thresholds) BSHAA Congress - Telford 15 th May 2015

Aim To assess for the first time the contribution of the vestibular organ to the long-latency auditory evoked potentials of cortical origin, using air conducted stimuli presented at intensities below and above the vestibular threshold (VT) BSHAA Congress - Telford 15 th May 2015

Subjects • 14 healthy adults (mean age= 28. 3; SD=6. 9, 5 females, 9 males) Stimuli • 2 -ms, 500 -Hz single cycle tone pips • Played via EAR-3 A inserts • RMS SPL of 115. 4 d. B re 20 u. Pa BSHAA Congress - Telford 15 th May 2015

Auditory and Vestibular Thresholds • Auditory thresholds measured using 3 -AFC method with 1 -d. B final step size • Vestibular thresholds measured using c. VEMP: – up to 200 stimuli were presented at a rate of 6 Hz – 5 d. B step size – Threshold defined as the smallest intensity at which a c. VEMP could be produced in at least two trials. BSHAA Congress - Telford 15 th May 2015

EEG recording • Subjects comfortably seated, watching silent movies. • Air-conducted tone pips played randomly between 600 and 1000 ms, up to 400 per trial. • Stimulus intensity always relative to vestibular threshold and presented at -24, -18, -12, -6, 0, +6, +12, +18 d. B re VT. BSHAA Congress - Telford 15 th May 2015

EEG recording • EEG was recorded using a 64 -channel EEG system (Biosemi, Inc. , USA). • Additional electrodes were also placed below each eye (i. e. infra-ocular electrodes, IO 1 and IO 2), at deep frontal (F 9 and F 10) and at earlobe locations (A 1 and A 2). BSHAA Congress - Telford 15 th May 2015

Results VEMP thresholds (mean, SD): Auditory thresholds: • Left ear: 108. 7 (6. 1) d. B pk. SPL • Left ear: 26 (5. 3) pk. SPL • Right ear: 109. 3 (6. 5) d. B pk. SPL • Right ear: 26. 2 (4. 1) pk. SPL VEMP thresholds in Sensation Level: Left ear 82. 7 d. BSL Right ear 83. 1 d. BSL BSHAA Congress - Telford 15 th May 2015

Grand means of EPs produced by 500 -Hz 2 -ms pips in standard 10 -20 locations, plus infra-ocular (IO) and aurcle (A) leads, for +18 d. B re. VT (dark trace) and -6 d. B re. VT (light trace) BSHAA Congress - Telford 15 th May 2015

Sub VT FCz channel (midline fronto-central) For signal below VT typical ABR wave V, Na, Pa, Nb, Pb/P 1, N 1, P 2 waves were recorded BSHAA Congress - Telford 15 th May 2015

Short, Middle and Late- Latency Auditory Evoked Potentials BSHAA Congress - Telford 15 th May 2015

Supra VT FCz channel (midline fronto-central) For signal above VT ADDITIONAL later waves not previously described were also observed BSHAA Congress - Telford 15 th May 2015

Middle and Late- Latency VESTIBULAR Evoked Potentials BSHAA Congress - Telford 15 th May 2015

Transition from Nb/Pb to N*/P* when passing through VEMP threshold -6 d. B re VT +18 d. B re VT N* P* BSHAA Congress - Telford 15 th May 2015

MLR peak-peak amplitudes - sig increase in slope when passing through VT LLR peak-peak amplitudes – NO sig increase in slope when passing through VT p=0. 042 p=0. 003 BSHAA Congress - Telford 15 th May 2015

Changes in response Latency with stimulus intensity No sig effects – Intensity function had reached its asymptote for these waves. significant main effect of intensity (F(5, 65) = 6. 7, p <. 01) significant main effect of intensity (F(5, 65) = 5. 2, p <. 05) BSHAA Congress - Telford 15 th May 2015

Unilaterally avestibular patient BSHAA Congress - Telford 15 th May 2015

Conclusions • For 500 -Hz AC-stimuli there are systematic changes that take place in LAEPs at intensities above the VEMP threshold • New mid-latency potential which appears to have a significant vestibular contribution (N*/P* at 42 ms/52 ms). • Changes in the slope of the amplitude functions with intensity of the AC stimulus and changes in the morphology and distribution of the potentials above and below VT. BSHAA Congress - Telford 15 th May 2015

Vestibular receptors contribute to cortical auditory evoked potentials The existence of a vestibular contribution to AEPs has at least two important consequences: 1. Any auditory studies (including MRI studies), which use high signal intensity need to take into account the possibility that results could be contaminated with non-cochlear i. e. vestibular contributions BSHAA Congress - Telford 15 th May 2015

Vestibular receptors contribute to cortical auditory evoked potentials The existence of a vestibular contribution to AEPs has at least two important consequences: 2. Acoustically activated non-cochlear (vestibular) projections may play a role in normal hearing, i. e. vestibular activation could contribute to the affective responses to sound or in listening to music and could have contributed to the evolution of music. BSHAA Congress - Telford 15 th May 2015

Acknowledgements • • Neil Todd Wellcome Trust Project Grant Aurore Paillard WT 091961 MA Elizabeth Whittle James Colebatch Aisha Mc. Lean A&D team in Manchester, UK Vestibular Lab team in Sydney, Australia Wonderful volunteers BSHAA Congress - Telford 15 th May 2015