Arch. Oto Rhino-Laryng. 212, 293-299 (1976)
Archives of Oto-Rhino-Laryngology
9 by Springer-Verlag1976
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss J. Tonndorf Department of Otolaryngology, College of Physicians and Surgeons of Columbia University, New York, 630 West 169th Street, New York, N.Y. 10032, USA
Summary. An explanation for the mechanical origin of the hearing loss in endo lymphatic hydrops is presented that is based on studies in mechanical cochlear models. An elastic bias of the basilar membrane and/or a mass loading of the cochlear duct account for the low-frequency hearing loss, diplacusis, and evenharmonic distortion. In addition, the static shearing displacement between the tectorial membrane and the organ of Corti, caused by the displacement of the basilar membrane, may partially decouple the hair cells from the tectorial membrane, an event that would explain the tinnitus, recruitment, and perhaps even the disportional loss of speech intelligibility associated with endolymphatic hydrops. Key words: Endolymphatic hydrops - Hearing loss - Endolymphatic/perilymphatic pressure difference
The hearing loss observed during acute episodes of endolymphatic hydrops in the early stages of the disease is of the low-frequency, fluctuating type. This fact sug gests that the hearing loss might vary in some proportion to the endolymphatic/perilymphatic pressure difference or to the volume of the cochlear duct; in other words it might be of purely mechanical origin. The first question that must then be asked is whether the membranous structures separating the two cochlear fluid compartments are elastic or not. (Although from the biochemical standpoint the separation is given by Reissner's membrane on one side and the reticular membrane on the other, from the structural standpoint, the restoring force of the partition between scala media and scala tympani is determined by properties of the basilar membrane). That the basilar membrane is indeed an elastic structure is well known from B+k+sy's original measurements (1928). Its compliance varies systematically from base to apex, a fact that was amply confirmed by numerous findings in cochlear dynamics, i.e., it is the stiffness gradient of
294
J. Tonndorf
the basilar membrane that is the basic structural property required for the generation of traveling waves of the B~k~sy type. An elastic behavior of Reissner's membrane was accidently observed in the guinea pig (Tonndorf et al., 1962). Finally, Hendriksson (1968) demonstrated in the frog that the entire endolymphatic system reacts in an elastic manner. However, it appears that Reissner's membrane is elastic only a long as its distention does not last for too long a time. Kimura (1968) produced endolymphatic hydro!0s experimentally in cats. He observed in several of his specimens spontaneous ruptures of Reissner's membrane. The histological findings suggested that these ruptures had occurred during life. In one or two instances Reissner's membrane had returned to its resting position, i.e., it had retained its elastic properties. In some others, it had not done so, but had remained in its distended position; hence, these membranes had been overextended in a viscous manner. This finding is not surprising. Most biological (connective-tissue) membranes possess visco-elastic properties. That is to say, on shortlasting distentions, they react mainly in an elastic manner, but with increasing time durations the viscous component comes more and more to the fore. Whether or not the basilar membrane is also a visco-elastic membrane (as it might well be) is a moot point from the standpoint of the present inquiry. As soon as the less resistant of the two membranes becomes over-extended - which is obviously Reissner's membrane - the endolymphatic system as a whole can no longer be elastically biased; it will then be merely mass-loaded. Thus, during acute hydrops episodes, the dominant factor from the present standpoint is the endolymphatic/perilymphatic pressure difference, with the volume increment of the cochlear duct playing a lesser role. Under chronic conditions, the volume increment of the cochlear duct is the sole governing factor. Experiments were conducted in cochlear models that were equipped with two elastic membranes (Tonndorf, 1957). Figure 1 shows the static displacement of the basilar membrane; the shape is a direct consequence of the stiffness gradient. Reissner's membrane was made uniformly compliant, but less stiff than the basilar membrane. In these models, low-frequency sensitivity losses were demonstrated that were in some proportion to the prevailing pressure differences across the basilar membrane (Fig. 2). Futhermore, the places of maximal displacement of the traveling waves were shifted, which must be considered the equivalent of diplacusis (Fig. 3). Finally, there was even-harmonic distortion (Fig. 4), a well-known feature of Meni~re's disease (Opheim and Flottorp, 1955).
cps o
4o0
~co
=~" ! I0 .~a
> ioo
50
25
'
,
,
20 rnrn. DISTANCE
3~0 )"
Fig. 1. Cochlear model: Static displacement of the basilar membrane caused by an increase in endolymphatic fluid volume. Note that in all experiments volume increments instead of pressure differences were measured for the sake of convenience. Lower scale: distance along the partition. Upper scale: places of f/eqtiency maxima when there is no change in the endolymphatic fluid volume (from Tonndorf, 1957)
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss FREQUENCY 25
=
50
(cps) tO0
o/./~
I 4 r;
295
200
400
/ 9/
VOLU
l
EMENT x 10.2 % 13.6% m 17.0% 9 20.4 %
7 8
Fig. 2. Cochlear model: Loss in sensitivity of the basilar membrane as a function of increases in endolymphatic fluid volume (from Tonndorf~ 1957)
l 9 E
40~-
3o[!.
~
?-5 Cps ~
~
.
.
VOLUME
.
.
.
.
~o
INCREMENT
(%)
I 0 0 cps
Fig. 3. Cochlear model: Shifts of the place of frequency maxima as a function of increases in endolymphatic fluid volume (from T0nndorf, !957)
The sensitivity losses of Figure 2 could have been caused either by the elastic bias of the basilar m e m b r a n e or by the mass loading of the cochlear duct. To decide the issue, sensitivity changes were also determined when the endolymphatic fluid volume was decreased. The elastic bias was the same under both conditions. The changes were quite similar to those obtained in the first experiment, indicating that the elastic bias was responsible in both instances. The type of sensitivity loss observed in the models was duplicated in a number of acute animals studies in which the endolymphatic/perilymphatic pressure difference was varied experimentally and the change in cochlear microphonic responses used as an indicator ( M c C a b e and Wolsk, 1961; Allen and Habibi, 1962; Simmons, 1968). Moreover, K i m u r a (1968) found similar low-frequency changes o f cochlear microphonic responses in his chronic preparations.
J. Tonndorf
296 A
B
0s0 emeo (--)Applied Force(+-)
.
.
.
.
.
(-)Applied Force(+)
Fig. 4. Vibratory characteristics of an elastic membrane (schematic cross-section). A: Unbiased. B: elastically biased. The force/displacement diagram below shows the nonlinear limitations of unbiased membranes (case A), eventually leading to odd-harmonic distortion at high amplitudes. If such a membrane is biased (case B) its operating point is shifted and the characteristic becomes asymmetrical as indicated. As a consequence there is even-harmonic distortion at relatively low amplitudes. Such distortions were actually observed in the model (from Tonndorf, 1968)
The diplacusis-like shifts of Figure 3 occurred in the direction of the cochlear base. The latter shifts were caused by mass loading. An increase in mass of individual elements along the partition detunes them, lowering their frequencies so that the traveling-wave maxima are formed in more proximal places. Had they been caused by the pressure difference across the partition, the shifts should have occurred toward the cochlear apex because the type of static displacement shown in Figure 1 tends to make the stiffness gradient less steep; and that in turn lets the position of frequency spread out in distance. The difference between the two cases is merely a matter of the stiffness ratio between Reissner's membrane and the basilar membrane. Had the Reissner's membrane of the model been relatively stiffer, the frequency shifts would have occurred toward the cochlear apex, since a smaller volume increment would have sufficed to produce the same elastic bias. In this respect, the report of an otolaryngologist, Dr. R. V. G., himself afflicted with Menibre's disease, might be of interest. Dr. G. stated that during acute episodes, the pitch in his involved ear first becomes higher than that in the other one (elastic bias); later on, when the attack subsides, the pitch becomes lower (mass bias). Apparently then, some viscous changes of Reissner's membrane must occur in his ear with time. Figure 5 summarizes the present findings with respect to the acute episodes (left side) and extends them to the case of the chronic condition (right side). As soon as the mass bias becomes the sole governing factor, there is a flat sensitivity loss; diplacusis is also present, with the shifts taking place in the direction of the cochlear apex, i.e., toward lower frequencies; distortion does not occur anymore because the membranes are no longer elastically biased. At the time these model studies were conducted (1957), it appeared that some additional signs and symptoms of Meni~re's disease, tinnitus, recruitment, and the disproportionate loss of speech intelligibility could not be accounted for on the basis of the mechanical changes described. Some recent, independent findings by Bredberg et al. (1972) provided new clues in these respects. These authors, with the aid of scanning electronmicroscopy, observed bleb-like lesions that formed on the apical ends of the cochlear stereocilia after noise exposure. (Such blebs are occasionally seen in normal, healthy animals, but their inci-
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss
Fig. 5. Unclipped (A) and center clipped (B, C) waveforms. Waveform C is 10 dB larger than waveform B. The amount of center clipping is the same in both cases. Note that with increasing amplitude the effect of constant center clipping becomes gradually less so that the input/output function attains the shape shown by the curve on Figure (D)
297
v
o_
o I N P U T (10g)
dence increased markedly after noise exposure). Behavioral tests conducted in these animals (cats) prior to sacrifice had revealed hearing losses that were considerably more severe than what would have been predicted on the basis of hair-cell losses demonstrated by light microscopy. The above observations indicate that the blebs when present on the stereocilia partially decoupie the connection between the tectorial membrane and the hair cells. This conclusion offers an explanation for tinnitus of cochlear origin. Harris (1968) calculated the effects of the Brownian motion of the air particles in front of the tympanic membrane upon the noise level at the hair cell input. He found that his calculations depended greatly on the degree of coupling between the hair cells and the tectorial membrane. For tight coupling, he obtained a noise level o f - 2 2 dB in reference to the normal auditory threshold, indicating that this threshold is given by the prevailing S/N ratio as are most other such "thresholds". For loose coupling, Harris found the noise level at the hair-cell input to increase to +33 dB in reference to the auditory threshold. In 1968, Harris had of course no notion of Bredberg's 1972 observations and their implications for his own results. We are now in a position to conclude that the increased noise level at the hair cell input, an increment of 55 dB, that is caused by the partial decoupling of the stereocilia from the tectorial membrane, ought to be perceived as tinnitus. We may now return to the present problem. The static displacement of the basilar membrane that is brought about during acute episodes of endolymphatic hydrops (elastic bias) produces a shearing displacement between the tectorial membrane and the organ of Corti. This static shear should over-extend the tenuous junctions between the stereocilia and the tectorial membrane, likewise leading to a partial decoupling of these junctions. Not only will the decoupling increase the de-
298
J. Tonndorf
gree of the sensitivity loss, as observed in Bredberg's animals, but it might also account for the occurrence of tinnitus, recruitment, and, perhaps even, for the loss oJ"
speech intelligibility. The tinnitus comes about in exactly the same manner as that just described for the case of a noise trauma. Meni+re patients usually describe their tinnitus as "roaring". The following explanation is offered: The Brownian motion in front of the tympanic membrane produces a broad-band noise. However, when this noise enters the cochlea, its frequency components are distributed along the partition in accordance with the place principle. Decoupling is maximal in the region where the basilar membrane displacement is largest, i.e., in the apical region (cf. Fig. 1). The noise must therefore be perceived as a band-limited, tow-frequency noise, i.e., as "roaring". The best way to demonstrate recruitment in normal hearing subjects is by applying center-clipped signals. Figure 5 shows one unclipped and two center-clipped waveforms. A comparison of waveforms B and C indicates that a constant amount of center-clipping becomes less apparent as signal amplitude is increased. The input/output function therefore follows the curve of Figure 5 D which closely resembles a recruitment curve. Partial, mechanical decoupling means that the tectorial membrane has to move a certain distance in either direction before establishing firm contact with the stereocilia. In other words, there is a certain amount of "play" around the center position, which is the essence of center-clipping. In his skin analogy studies B~k~sy (1957) demonstrated recruitment whenever the density of sensory receptors was less than normal. There can be no doubt that this is one of the causes of cochlear recruitment. It should occur whenever a number of hair cells are permanently missing or are completely non-functional. However, it does not account for the transient recruitment found dm:ing acute episodes of cochlear hydrops which is better explained by the present concept. With respect to the disproportional loss of speech perception associated with acute hydrops episodes, the evidence is less clear. One may of course argue that if during a given hydrops episode the pure tone loss, the recruitment, and the speech loss follow essentially the same time course, as they in fact do, then in all probability they ought to be tied to the same (mechanical) cause. The two phenomena one might a priori suspect of being responsible for the speech loss are (a) the center-clipping, the proposed cause of recruitment, and (b) the masking produced by the tinnitus. It is well known that neither of them by itself affects speech intelligibility to a large disproportionate degree in normal ears. Nevertheless, a case could be made for their combined action inpathologieal ears. It is a common audiological experience that masking impairs the hearing of speech more than that of pure tones whenever the number of available neural channels is reduced, e.g., after a neuronitis of the 8th nerve. The partial decoupling of the hair cells from the tectorial membrane, as it was described above, reduces the number of available sensory cell inputs, expecially at low-signal levels. What we simply do not know at this point is whether or not the reduction of input channels (hair cells) has the same effect in this regard as the reduction of transmission channels (nerve fibers).
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss
299
References Allen, G., Habibi, M.: Laryngoscope 72, 423--434 (1962) B+k+sy, G. yon: Experiments in Hearing. p. 793-810, New York: McGraw Hill 1960 B+k+sy, G. yon: Experiments in Hearing~ p. 568 609, New York: McGraw Hill 1960 Bredberg, G., Ades, H. W., Engstr6m, H.: Acta Otolaryng., Suppl. 301, 3--48 (1972) Harris, G. G.: J. acoust. Soc. Amer. 44, 176--186 (1968) Hendriksson. N. G.: Meni~re's Disease (J. Pulec, Ed.), p. 373-368, Philadelphia: Saunders 1968 Kimura, R.: Meni~re's Disease (J. Pulec, Ed.), p. 457 472, Philadelphia: Saunders 1968 McCabe, B., Wolsk, J.: Ann. Oto-laryng. 70, 541 555 (1961) Opheim, O., Flottorp, G.: Acta Oto-laryng. 45, 513-531 (1955) Simmons. F. B.: Meni&e's Disease (J. Pulec, Ed.), p. 473--478, Philadelphia: Saunders 1968 Tonndorf, J.: Ann. Oto-iaryng. 66, 766-784 (1957) Tonndoff. J.: Meni&e's Disease (J. Pulec, Ed.), p. 375-388, Philadelphia: Saunders 1968
Diskussionsbemerkungen J. Wers~ill (Stockholm): Wie lange kann die Membran dem Druck Widerstand leisten? Kann eine fiberdehnte Membran oder eine geborstene wieder normale Funktionen erffillen? J. Tonndorf (New York): Aufgrund meiner Modellversuche lfiSt sich diese Frage nicht beantworten. Aber die Elastizit~t ist sicher verfindert naeh starker (Jberdehnung. Es spielt auch eine Rolle, wie lange die Membran verschoben war. Ob zum Zeitpunkt der Ruptur die Elastizit~it der Membran erhalten ist oder nicht, kann ich nicht sagen. J. E. Hawkins (Ann Arbor): In unseren Hydropsf/~Ilen scheinen die Membranen dutch Zellwachstum verI~ngert und nicht durch Druck zerdehnt. Das Wachstum verlangt lange Zeit. R. S. Kimura (Boston): Haben Sic vermehrte Zellzahlen bzw. Kerne gesehen?
J. E. Hawkins (Ann Arbor): Ja. J. Kloekhoff (Uppsala): Die zerdehnte Membran hat andere Trenn- und Elastizk~itseigenschaften. stimmt das? J. Tonndorf (New York): Ja, aus einer elastischen wird eine visco-dastische Membran. H. F. Schukneeht (Boston): Die Membran /indert ihre zellulfiren und mechanischen Eigenschaften. R. S. Kimura (Boston): Zerdehnte Membranen zeigen fehlende Mesothelien und die Reil3nersche Mere bran ist in den nicht hydropischen Teilen der Kochlea dicker als am Apex. H. F. Schukneeht (Boston): Meinen Sic, dab Gewichts- oder Druckerh6hung beim chronischen Hy drops den H6rverlust in allen Frequenzen verursacht? J. Tonndorf (New York): Nein, ich spreehe von einer Fl/issigkeitszunahme im System und damit von einer Verschiebung des ganzen Ductus cochlearis. J. Wers~ill (Stockholm): Haben Sic Volumenmessungen an der ReiBnerschen Membran gemacht, Zellen gez~ihlt?
H. F. Schukneeht (Boston): Es ist sehr schwer, da die Membran ja meistens nach der Dehnung dem kn6chernen Labyrinth anliegt.
Archives of Oto-Rhino-Laryngology
9 by Springer-Verlag1976
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss J. Tonndorf Department of Otolaryngology, College of Physicians and Surgeons of Columbia University, New York, 630 West 169th Street, New York, N.Y. 10032, USA
Summary. An explanation for the mechanical origin of the hearing loss in endo lymphatic hydrops is presented that is based on studies in mechanical cochlear models. An elastic bias of the basilar membrane and/or a mass loading of the cochlear duct account for the low-frequency hearing loss, diplacusis, and evenharmonic distortion. In addition, the static shearing displacement between the tectorial membrane and the organ of Corti, caused by the displacement of the basilar membrane, may partially decouple the hair cells from the tectorial membrane, an event that would explain the tinnitus, recruitment, and perhaps even the disportional loss of speech intelligibility associated with endolymphatic hydrops. Key words: Endolymphatic hydrops - Hearing loss - Endolymphatic/perilymphatic pressure difference
The hearing loss observed during acute episodes of endolymphatic hydrops in the early stages of the disease is of the low-frequency, fluctuating type. This fact sug gests that the hearing loss might vary in some proportion to the endolymphatic/perilymphatic pressure difference or to the volume of the cochlear duct; in other words it might be of purely mechanical origin. The first question that must then be asked is whether the membranous structures separating the two cochlear fluid compartments are elastic or not. (Although from the biochemical standpoint the separation is given by Reissner's membrane on one side and the reticular membrane on the other, from the structural standpoint, the restoring force of the partition between scala media and scala tympani is determined by properties of the basilar membrane). That the basilar membrane is indeed an elastic structure is well known from B+k+sy's original measurements (1928). Its compliance varies systematically from base to apex, a fact that was amply confirmed by numerous findings in cochlear dynamics, i.e., it is the stiffness gradient of
294
J. Tonndorf
the basilar membrane that is the basic structural property required for the generation of traveling waves of the B~k~sy type. An elastic behavior of Reissner's membrane was accidently observed in the guinea pig (Tonndorf et al., 1962). Finally, Hendriksson (1968) demonstrated in the frog that the entire endolymphatic system reacts in an elastic manner. However, it appears that Reissner's membrane is elastic only a long as its distention does not last for too long a time. Kimura (1968) produced endolymphatic hydro!0s experimentally in cats. He observed in several of his specimens spontaneous ruptures of Reissner's membrane. The histological findings suggested that these ruptures had occurred during life. In one or two instances Reissner's membrane had returned to its resting position, i.e., it had retained its elastic properties. In some others, it had not done so, but had remained in its distended position; hence, these membranes had been overextended in a viscous manner. This finding is not surprising. Most biological (connective-tissue) membranes possess visco-elastic properties. That is to say, on shortlasting distentions, they react mainly in an elastic manner, but with increasing time durations the viscous component comes more and more to the fore. Whether or not the basilar membrane is also a visco-elastic membrane (as it might well be) is a moot point from the standpoint of the present inquiry. As soon as the less resistant of the two membranes becomes over-extended - which is obviously Reissner's membrane - the endolymphatic system as a whole can no longer be elastically biased; it will then be merely mass-loaded. Thus, during acute hydrops episodes, the dominant factor from the present standpoint is the endolymphatic/perilymphatic pressure difference, with the volume increment of the cochlear duct playing a lesser role. Under chronic conditions, the volume increment of the cochlear duct is the sole governing factor. Experiments were conducted in cochlear models that were equipped with two elastic membranes (Tonndorf, 1957). Figure 1 shows the static displacement of the basilar membrane; the shape is a direct consequence of the stiffness gradient. Reissner's membrane was made uniformly compliant, but less stiff than the basilar membrane. In these models, low-frequency sensitivity losses were demonstrated that were in some proportion to the prevailing pressure differences across the basilar membrane (Fig. 2). Futhermore, the places of maximal displacement of the traveling waves were shifted, which must be considered the equivalent of diplacusis (Fig. 3). Finally, there was even-harmonic distortion (Fig. 4), a well-known feature of Meni~re's disease (Opheim and Flottorp, 1955).
cps o
4o0
~co
=~" ! I0 .~a
> ioo
50
25
'
,
,
20 rnrn. DISTANCE
3~0 )"
Fig. 1. Cochlear model: Static displacement of the basilar membrane caused by an increase in endolymphatic fluid volume. Note that in all experiments volume increments instead of pressure differences were measured for the sake of convenience. Lower scale: distance along the partition. Upper scale: places of f/eqtiency maxima when there is no change in the endolymphatic fluid volume (from Tonndorf, 1957)
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss FREQUENCY 25
=
50
(cps) tO0
o/./~
I 4 r;
295
200
400
/ 9/
VOLU
l
EMENT x 10.2 % 13.6% m 17.0% 9 20.4 %
7 8
Fig. 2. Cochlear model: Loss in sensitivity of the basilar membrane as a function of increases in endolymphatic fluid volume (from Tonndorf~ 1957)
l 9 E
40~-
3o[!.
~
?-5 Cps ~
~
.
.
VOLUME
.
.
.
.
~o
INCREMENT
(%)
I 0 0 cps
Fig. 3. Cochlear model: Shifts of the place of frequency maxima as a function of increases in endolymphatic fluid volume (from T0nndorf, !957)
The sensitivity losses of Figure 2 could have been caused either by the elastic bias of the basilar m e m b r a n e or by the mass loading of the cochlear duct. To decide the issue, sensitivity changes were also determined when the endolymphatic fluid volume was decreased. The elastic bias was the same under both conditions. The changes were quite similar to those obtained in the first experiment, indicating that the elastic bias was responsible in both instances. The type of sensitivity loss observed in the models was duplicated in a number of acute animals studies in which the endolymphatic/perilymphatic pressure difference was varied experimentally and the change in cochlear microphonic responses used as an indicator ( M c C a b e and Wolsk, 1961; Allen and Habibi, 1962; Simmons, 1968). Moreover, K i m u r a (1968) found similar low-frequency changes o f cochlear microphonic responses in his chronic preparations.
J. Tonndorf
296 A
B
0s0 emeo (--)Applied Force(+-)
.
.
.
.
.
(-)Applied Force(+)
Fig. 4. Vibratory characteristics of an elastic membrane (schematic cross-section). A: Unbiased. B: elastically biased. The force/displacement diagram below shows the nonlinear limitations of unbiased membranes (case A), eventually leading to odd-harmonic distortion at high amplitudes. If such a membrane is biased (case B) its operating point is shifted and the characteristic becomes asymmetrical as indicated. As a consequence there is even-harmonic distortion at relatively low amplitudes. Such distortions were actually observed in the model (from Tonndorf, 1968)
The diplacusis-like shifts of Figure 3 occurred in the direction of the cochlear base. The latter shifts were caused by mass loading. An increase in mass of individual elements along the partition detunes them, lowering their frequencies so that the traveling-wave maxima are formed in more proximal places. Had they been caused by the pressure difference across the partition, the shifts should have occurred toward the cochlear apex because the type of static displacement shown in Figure 1 tends to make the stiffness gradient less steep; and that in turn lets the position of frequency spread out in distance. The difference between the two cases is merely a matter of the stiffness ratio between Reissner's membrane and the basilar membrane. Had the Reissner's membrane of the model been relatively stiffer, the frequency shifts would have occurred toward the cochlear apex, since a smaller volume increment would have sufficed to produce the same elastic bias. In this respect, the report of an otolaryngologist, Dr. R. V. G., himself afflicted with Menibre's disease, might be of interest. Dr. G. stated that during acute episodes, the pitch in his involved ear first becomes higher than that in the other one (elastic bias); later on, when the attack subsides, the pitch becomes lower (mass bias). Apparently then, some viscous changes of Reissner's membrane must occur in his ear with time. Figure 5 summarizes the present findings with respect to the acute episodes (left side) and extends them to the case of the chronic condition (right side). As soon as the mass bias becomes the sole governing factor, there is a flat sensitivity loss; diplacusis is also present, with the shifts taking place in the direction of the cochlear apex, i.e., toward lower frequencies; distortion does not occur anymore because the membranes are no longer elastically biased. At the time these model studies were conducted (1957), it appeared that some additional signs and symptoms of Meni~re's disease, tinnitus, recruitment, and the disproportionate loss of speech intelligibility could not be accounted for on the basis of the mechanical changes described. Some recent, independent findings by Bredberg et al. (1972) provided new clues in these respects. These authors, with the aid of scanning electronmicroscopy, observed bleb-like lesions that formed on the apical ends of the cochlear stereocilia after noise exposure. (Such blebs are occasionally seen in normal, healthy animals, but their inci-
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss
Fig. 5. Unclipped (A) and center clipped (B, C) waveforms. Waveform C is 10 dB larger than waveform B. The amount of center clipping is the same in both cases. Note that with increasing amplitude the effect of constant center clipping becomes gradually less so that the input/output function attains the shape shown by the curve on Figure (D)
297
v
o_
o I N P U T (10g)
dence increased markedly after noise exposure). Behavioral tests conducted in these animals (cats) prior to sacrifice had revealed hearing losses that were considerably more severe than what would have been predicted on the basis of hair-cell losses demonstrated by light microscopy. The above observations indicate that the blebs when present on the stereocilia partially decoupie the connection between the tectorial membrane and the hair cells. This conclusion offers an explanation for tinnitus of cochlear origin. Harris (1968) calculated the effects of the Brownian motion of the air particles in front of the tympanic membrane upon the noise level at the hair cell input. He found that his calculations depended greatly on the degree of coupling between the hair cells and the tectorial membrane. For tight coupling, he obtained a noise level o f - 2 2 dB in reference to the normal auditory threshold, indicating that this threshold is given by the prevailing S/N ratio as are most other such "thresholds". For loose coupling, Harris found the noise level at the hair-cell input to increase to +33 dB in reference to the auditory threshold. In 1968, Harris had of course no notion of Bredberg's 1972 observations and their implications for his own results. We are now in a position to conclude that the increased noise level at the hair cell input, an increment of 55 dB, that is caused by the partial decoupling of the stereocilia from the tectorial membrane, ought to be perceived as tinnitus. We may now return to the present problem. The static displacement of the basilar membrane that is brought about during acute episodes of endolymphatic hydrops (elastic bias) produces a shearing displacement between the tectorial membrane and the organ of Corti. This static shear should over-extend the tenuous junctions between the stereocilia and the tectorial membrane, likewise leading to a partial decoupling of these junctions. Not only will the decoupling increase the de-
298
J. Tonndorf
gree of the sensitivity loss, as observed in Bredberg's animals, but it might also account for the occurrence of tinnitus, recruitment, and, perhaps even, for the loss oJ"
speech intelligibility. The tinnitus comes about in exactly the same manner as that just described for the case of a noise trauma. Meni+re patients usually describe their tinnitus as "roaring". The following explanation is offered: The Brownian motion in front of the tympanic membrane produces a broad-band noise. However, when this noise enters the cochlea, its frequency components are distributed along the partition in accordance with the place principle. Decoupling is maximal in the region where the basilar membrane displacement is largest, i.e., in the apical region (cf. Fig. 1). The noise must therefore be perceived as a band-limited, tow-frequency noise, i.e., as "roaring". The best way to demonstrate recruitment in normal hearing subjects is by applying center-clipped signals. Figure 5 shows one unclipped and two center-clipped waveforms. A comparison of waveforms B and C indicates that a constant amount of center-clipping becomes less apparent as signal amplitude is increased. The input/output function therefore follows the curve of Figure 5 D which closely resembles a recruitment curve. Partial, mechanical decoupling means that the tectorial membrane has to move a certain distance in either direction before establishing firm contact with the stereocilia. In other words, there is a certain amount of "play" around the center position, which is the essence of center-clipping. In his skin analogy studies B~k~sy (1957) demonstrated recruitment whenever the density of sensory receptors was less than normal. There can be no doubt that this is one of the causes of cochlear recruitment. It should occur whenever a number of hair cells are permanently missing or are completely non-functional. However, it does not account for the transient recruitment found dm:ing acute episodes of cochlear hydrops which is better explained by the present concept. With respect to the disproportional loss of speech perception associated with acute hydrops episodes, the evidence is less clear. One may of course argue that if during a given hydrops episode the pure tone loss, the recruitment, and the speech loss follow essentially the same time course, as they in fact do, then in all probability they ought to be tied to the same (mechanical) cause. The two phenomena one might a priori suspect of being responsible for the speech loss are (a) the center-clipping, the proposed cause of recruitment, and (b) the masking produced by the tinnitus. It is well known that neither of them by itself affects speech intelligibility to a large disproportionate degree in normal ears. Nevertheless, a case could be made for their combined action inpathologieal ears. It is a common audiological experience that masking impairs the hearing of speech more than that of pure tones whenever the number of available neural channels is reduced, e.g., after a neuronitis of the 8th nerve. The partial decoupling of the hair cells from the tectorial membrane, as it was described above, reduces the number of available sensory cell inputs, expecially at low-signal levels. What we simply do not know at this point is whether or not the reduction of input channels (hair cells) has the same effect in this regard as the reduction of transmission channels (nerve fibers).
Endolymphatic Hydrops: Mechanical Causes of Hearing Loss
299
References Allen, G., Habibi, M.: Laryngoscope 72, 423--434 (1962) B+k+sy, G. yon: Experiments in Hearing. p. 793-810, New York: McGraw Hill 1960 B+k+sy, G. yon: Experiments in Hearing~ p. 568 609, New York: McGraw Hill 1960 Bredberg, G., Ades, H. W., Engstr6m, H.: Acta Otolaryng., Suppl. 301, 3--48 (1972) Harris, G. G.: J. acoust. Soc. Amer. 44, 176--186 (1968) Hendriksson. N. G.: Meni~re's Disease (J. Pulec, Ed.), p. 373-368, Philadelphia: Saunders 1968 Kimura, R.: Meni~re's Disease (J. Pulec, Ed.), p. 457 472, Philadelphia: Saunders 1968 McCabe, B., Wolsk, J.: Ann. Oto-laryng. 70, 541 555 (1961) Opheim, O., Flottorp, G.: Acta Oto-laryng. 45, 513-531 (1955) Simmons. F. B.: Meni&e's Disease (J. Pulec, Ed.), p. 473--478, Philadelphia: Saunders 1968 Tonndorf, J.: Ann. Oto-iaryng. 66, 766-784 (1957) Tonndoff. J.: Meni&e's Disease (J. Pulec, Ed.), p. 375-388, Philadelphia: Saunders 1968
Diskussionsbemerkungen J. Wers~ill (Stockholm): Wie lange kann die Membran dem Druck Widerstand leisten? Kann eine fiberdehnte Membran oder eine geborstene wieder normale Funktionen erffillen? J. Tonndorf (New York): Aufgrund meiner Modellversuche lfiSt sich diese Frage nicht beantworten. Aber die Elastizit~t ist sicher verfindert naeh starker (Jberdehnung. Es spielt auch eine Rolle, wie lange die Membran verschoben war. Ob zum Zeitpunkt der Ruptur die Elastizit~it der Membran erhalten ist oder nicht, kann ich nicht sagen. J. E. Hawkins (Ann Arbor): In unseren Hydropsf/~Ilen scheinen die Membranen dutch Zellwachstum verI~ngert und nicht durch Druck zerdehnt. Das Wachstum verlangt lange Zeit. R. S. Kimura (Boston): Haben Sic vermehrte Zellzahlen bzw. Kerne gesehen?
J. E. Hawkins (Ann Arbor): Ja. J. Kloekhoff (Uppsala): Die zerdehnte Membran hat andere Trenn- und Elastizk~itseigenschaften. stimmt das? J. Tonndorf (New York): Ja, aus einer elastischen wird eine visco-dastische Membran. H. F. Schukneeht (Boston): Die Membran /indert ihre zellulfiren und mechanischen Eigenschaften. R. S. Kimura (Boston): Zerdehnte Membranen zeigen fehlende Mesothelien und die Reil3nersche Mere bran ist in den nicht hydropischen Teilen der Kochlea dicker als am Apex. H. F. Schukneeht (Boston): Meinen Sic, dab Gewichts- oder Druckerh6hung beim chronischen Hy drops den H6rverlust in allen Frequenzen verursacht? J. Tonndorf (New York): Nein, ich spreehe von einer Fl/issigkeitszunahme im System und damit von einer Verschiebung des ganzen Ductus cochlearis. J. Wers~ill (Stockholm): Haben Sic Volumenmessungen an der ReiBnerschen Membran gemacht, Zellen gez~ihlt?
H. F. Schukneeht (Boston): Es ist sehr schwer, da die Membran ja meistens nach der Dehnung dem kn6chernen Labyrinth anliegt.
