Altoè, Alessandro

Pulkki, Ville

Verhulst, Sarah

English

Ghent University Academic Bibliography

23I SVC23rd International Congress on Sound & Vibration10-14 July 2016Athens, Greece THE TWO FUNCTIONS OF THE RETICULAR LAMINAAlessandro Altoè, Ville PulkkiAalto University, School of Electrical Engineering, Department of Acoustics and Signal Processing, 02150Espoo, Finlandemail: alessandro.altoe@aalto.fiSarah VerhulstOldenburg University, Cluster of Excellence Hearing4all, Department of Medical Physics and Acoustics, 26111Oldenburg, GermanyThe cell body of the outer hair cells connects the reticular lamina and the basilar membranethrough supporting cells. According to the predominant view of cochlear mechanics, the outer haircells enhance wave propagation in the scala media by dynamically expanding and contracting theirbody, thus providing an active driving force to the basilar membrane. In order to maximize theefficiency of such mechanism, the reticular lamina should behave like a rigid anchor; in this waythe force associated with the length change of the outer hair cells body is efficiently transmitted tothe basilar membrane. On the other hand, the motion of the reticular lamina provides a direct driveto the inner-hair cells through a fluid-cilia coupling mechanism. Therefore a free-to-move reticularlamina would be highly responsive to the activity of outer hair cells, thus locally enhancing thesensitivity of inner hair cells. Within this view, the reticular lamina should trade-off between thetwo conflicting requirements of 1) providing a firm attachment to the outer hair cells and 2) beingsensitive to outer hair cells motility. A different thesis, partially supported by recent recordingsof the intact organ of Corti, is that a longitudinal coupling of motion in the scala media (similaras in feed-forward cochlear models) allows for a simultaneous enhancement of basilar membraneand stereocilia vibrations without imposing contradicting requirements for the functioning of thereticular lamina. In this study, we discuss the recent experimental and theoretical findings underthis perspective.1. IntroductionAlthough most literature about cochlear mechanics focuses on the vibrations of the basilar mem-brane (BM), the relationship between BM vibration and hearing sensations is still far from established.In fact, the stereocilia of the inner hair cells (IHC), which are the mechanical receptors of the auditorysystem, are relatively distant from the BM and are positioned in proximity to structures of which thevibratory patterns have yet to be established.Figure 1 shows a simplified cross-section of the organ Corti to guide the reader through the fol-lowing discussion. In the classical view, the IHC’s stereocilia are deflected by the radial shear motionof reticular lamina (RL) and tectorial membrane (TM). In particular, because the IHC stereocilia arenot embedded in the TM, their deflection is caused by viscous drag with the fluid in the subtectorialspace, turning them into sensors of fluid velocity. The modern view is that the fluid-flow in the IHCsurroundings is determined by the different elements in the organ of Corti [1, 2, 3, 4].For a long time the discussion about the IHC mechanical excitation was about whether IHC tuningreflects that of the BM or whether the organ of Corti acts as a "second filter" enhancing the frequency1The 23rd International Congress of Sound and Vibrationselectivity of IHCs. Second filter theories have been highly disregarded for the last two decades, asin vivo recordings from sensitive preparation in the guinea-pig and the chinchilla base [5, 6] showedsimilar BM and neural tuning. However recently, second filter theories have been revived under a newperspective by studies showing a different tuning of the structure in proximity of the IHC than that ofthe BM (e.g. [7, 8]).Based on recordings from chinchilla and guinea-pig [5, 6], as well comparison of psychophysicaland BM tuning in humans [9] we can reasonably exclude that the differences between IHC and BMtuning are substantial. Nonetheless, the greater awareness that the structures near the stereocilia retaindifferent vibraton patterns that the BM requires to think that the objective of the active processes is toenhance vibrations near the IHC stereocilia, not that of the BM. Therefore, the functional role of theBM needs to be questioned because often cochlear mechanics theories tends to treat the vibrations ofthe BM as cochlear mechanics itself rather than a means to excite IHCs.Basilar MembraneReticular laminaTectorial MembraneIHCPillar cellsOHCsFluid flowFigure 1: Simplified cross section of the organ of Corti.2. Reticular lamina transverse motion can drive the inner hair cellsWithin the modern view of organ of Corti mechanics, the action of outer hair cells (OHCs) sig-nificantly contribute to determine IHC responses, since they are active elements that can provide astrong drive to IHC at low sound pressure levels [1]. This idea has been recently discussed by [4],who identified four distinct drives contributing in deflecting the IHC stereocilia bundles. These drivesoperate via compression and expansion of the gap between reticular lamina and tectorial membrane,which causes the fluid to flow in and out of the subtectorial space, along with the classical radial shearcoupling between tectorial membrane and stereocilia bundles. In particular it has been postulatedthat the OHC somatic motility pulls the RL up and down [4], creating a significant fluid-flow in thesubtectorial space which plays a major role in driving the IHC from low to moderate SPLs.From this idea, it is natural to question whether the primary function the OHC somatic motilityis to amplify BM vibrations, or to improve the sensitivity of sensory cells. If OHCs function is onlyto improve the IHC sensitivity, then the optimal transmission of energy from the OHCs to the IHC’sstereocilia happens if the BM acts a rigid support for the OHCs and the RL is free to pivot on the topof pillar cells.2 ICSV23, Athens (Greece), 10-14 July 2016The 23rd International Congress of Sound and Vibration3. Cochlear amplifier and OHC somatic motilityOne of the main characteristic of the active process of cochlear mechanics is the enhancementof BM longitudinal waves. The so-called cochlear amplifier does not only increase the amplitude ofthe BM waves, but has a dramatical effect in shaping the frequency selectivity of the hearing organ.The predominant view is that the cochlear amplifier is the result of the combined action of somaticmotility of OHCs and active motion of OHCs’s stereocilia-bundles [10].The active process can be modelled mathematically through an additional force proportional toBM velocity (negative damping), compensated by a delayed stiffness [11]. Since such mathematicalformulation can be explained through a delayed force proportional to the BM displacement, a localaction of OHCs somatic motility is in principle a good candidate to provide such explanation. Con-trary to what discussed in section 2, for the OHCs motility to exert a significant amount of force tothe BM, the RL needs to provide a fairly rigid attachment to the OHCs.4. Longitudinal coupling through reticular laminaThe fact that the OHCs are not perpendicular to the BM, lead to the development of the so-calledfeed-forward models of cochlear macro-mechanics [12, 13]. In these models the action of OHCs isto enhance the frequency selectivity of the BM by providing an active force term which propagatesfrom one cochlear partition to a more basal one.In vivo recordings from the guinea-pig organ of Corti show that the phase and amplitude of RLresponse seem to reflect the combination of BMmotion in the same longitudinal location with the onefrom 100 to 200 µm on a more basal location [8]. Such coupling distance, although similar to the onedetermined empirically in feedforward models of cochlear mechanics [12], cannot be accounted forby the OHCs orientation, as they can provide longitudinal coupling over much smaller distances (e.g.[13]). Plausible physical mechanisms providing such long-distance coupling are additional waves inthe TM [14, 15], or electrical coupling of OHCs [16].According to the recordings from [7, 8] showing a phase lead of about 90  of RL and BM in thesame partition, this longitudinal coupling can provide an additional force to displace the BM which isapproximatively in phase with BM velocity, to act as a negative damping.If these results are further confirmed experimentally, then the combined action of longitudinal BMwaves and RL through the active OHCs and passive supporting cells, can indeed explain the frequencyselectivity of the BM. This explanation does not require the RL to act as a rigid support for OHCs,because large RL vibrations would be beneficial for amplifying both BM waves and driving the IHC.5. ConclusionsThe recent theoretical and experimental advances in cochlear mechanics indicate that the localaction of OHC somatic motility to explain the frequency selectivity and sensitivity of the hearingorgan imposes two conflicting requirements to the RL. First, because the motion of the RL providesa connection from OHCs to IHC stereocilia through the fluid in the subtectorial space, the RL has tobe free to follow the OHCs motion in order to increase maximally the IHC sensitivity. Second, thecochlear amplification through a local action of OHC somatic motility requires that the RL providesa rigid anchor to the OHCs in order to increase maximally the sensitivity of the BM. These tworequirements are in conflict, requiring the RL and BM to trade-off between the two.Another hypothesis is that the mechanical basis for the cochlear amplifier consists of an activecoupling between cochlear partitions, as postulated by "feed-forward" models of cochlear mechanics(e.g. [12]). Such a feed-forward realization of the cochlear amplifier does not impose conflictingrequirements for the functioning of the RL. Additionally, it would not only serve to enhance wavepropagation in the scala media, but also to increase the sensitivity of the IHCs.ICSV23, Athens (Greece), 10-14 July 2016 3The 23rd International Congress of Sound and VibrationTo conclude, recent experimental studies in the guinea-pig [7, 8] and mouse [17] show oppositeresults about the phase relationship between BM and RL vibration. Therefore at this time it is notpossible to establish what is the precise mechanism behind the cochlear amplifier. In particular theguinea-pig studies that show higher peak frequency and phase lead of RL over BM [7, 8] are compat-ible with a feed-forward basis for the cochlear amplifier. The mouse study showing in-phase motionof RL and BM at the characteristic frequency [17] is of more difficult interpretation. In any case bothsets of studies point out that the cochlear active process amplify RL vibrations more than those of theBM, an aspect that need to be addressed by future cochlear mechanics models.AcknowledgmentsThis work was supported by the Academy of Finland, the Aalto ELEC doctoral school and by theDFG cluster of excellence EXC 1077/1 "Hearing4all".REFERENCES1. Mountain, D. C. and Cody, A. R. Multiple modes of inner hair cell stimulation, Hearing research, 132 (1),1–14, (1999).2. Steele, C. R. and Puria, S. Force on inner hair cell cilia, International journal of solids and structures, 42(21), 5887–5904, (2005).3. Steele, C. R., Boutet de Monvel, J. and Puria, S. A multiscale model of the organ of corti, Journal ofmechanics of materials and structures, 4 (4), 755–778, (2009).4. Guinan, J. J. How are inner hair cells stimulated? evidence for multiple mechanical drives, Hearingresearch, 292 (1), 35–50, (2012).5. Sellick, P., Patuzzi, R. and Johnstone, B. Measurement of basilar membrane motion in the guinea pig usingthe mössbauer technique, The journal of the acoustical society of America, 72 (1), 131–141, (1982).6. Narayan, S. S., Temchin, A. N., Recio, A. and Ruggero, M. A. Frequency tuning of basilar membrane andauditory nerve fibers in the same cochleae, Science, 282 (5395), 1882–1884, (1998).7. Chen, F., Zha, D., Fridberger, A., Zheng, J., Choudhury, N., Jacques, S. L., Wang, R. K., Shi, X. andNuttall, A. L. A differentially amplified motion in the ear for near-threshold sound detection, Natureneuroscience, 14 (6), 770–774, (2011).8. Ramamoorthy, S., Zha, D., Chen, F., Jacques, S. L., Wang, R., Choudhury, N., Nuttall, A. L. and Fridberger,A. Filtering of acoustic signals within the hearing organ, The Journal of Neuroscience, 34 (27), 9051–9058,(2014).9. Shera, C. A., Guinan, J. J. and Oxenham, A. J. Revised estimates of human cochlear tuning from otoacous-tic and behavioral measurements, Proceedings of the National Academy of Sciences, 99 (5), 3318–3323,(2002).10. Ashmore, J., et al. The remarkable cochlear amplifier, Hearing research, 266 (1), 1–17, (2010).11. Zweig, G. Finding the impedance of the organ of corti., The Journal of the Acoustical Society of America,89 (3), 1229–1254, (1991).12. Geisler, C. D. and Sang, C. A cochlear model using feed-forward outer-hair-cell forces, Hearing research,86 (1), 132–146, (1995).13. Lim, K.-M. and Steele, C. R. A three-dimensional nonlinear active cochlear model analyzed by the wkb-numeric method, Hearing research, 170 (1), 190–205, (2002).4 ICSV23, Athens (Greece), 10-14 July 2016The 23rd International Congress of Sound and Vibration14. Ghaffari, R., Aranyosi, A. J. and Freeman, D. M. Longitudinally propagating traveling waves of themammalian tectorial membrane, Proceedings of the National Academy of Sciences, 104 (42), 16510–16515, (2007).15. Lee, H. Y., Raphael, P. D., Park, J., Ellerbee, A. K., Applegate, B. E. and Oghalai, J. S. Noninvasive invivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in themouse cochlea, Proceedings of the National Academy of Sciences, 112 (10), 3128–3133, (2015).16. Zhao, H.-B. and Santos-Sacchi, J. Auditory collusion and a coupled couple of outer hair cells, Nature, 399(6734), 359–362, (1999).17. Ren, T., He, W. and Barr-Gillespie, P. G. Reverse transduction measured in the living cochlea by low-coherence heterodyne interferometry, Nature communications, 7, (2016).ICSV23, Athens (Greece), 10-14 July 2016 5

The two functions of the reticular lamina

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The two functions of the reticular lamina

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