|Titel:||6.1.2(2). Olivocochlear efferents - Anatomy and Function||dutch version|
Editorial note: This chapter on the olivocochlear efferents has been written preliminary in English, in order to ask professor John Guinan Jr. (Harvard Medical School, Boston Massachusetts) his opinion on the chapter text and on the permissions in relation to the use of the illustrations. The chapter is available both in English and Dutch now. In this English version the texts within the illustrations are given in Dutch. The editors think that this, in combination with the ‘surrounding’ text, will be no problem.
The Editorial Board of the Textbook greatly appreciates that professor John Guinan Jr. (Harvard Medical School, Boston Massachusetts) has commented this chapter and has given valuable advices on the use of the illustrations.
Most information on the olivocochlear efferents described in this chapter has been obtained from the paper ‘Olivocochlear Efferents: Anatomy, Physiology, Function, and the Measurement of Efferent Effects in Humans’ by Guinan J.J. and from the textbook ‘An Introduction to the Physiology of Hearing’ (2008) by James O. Pickles.
The auditory pathway is a huge and complex system of bundles of neurons, which send information from the cochlea to higher auditory nuclei. These are called ‘afferent’ bundles, consisting of ‘afferent’ neurons. The afferent neurons are connected with the bases of the inner hair cells via about 30.000 ganglion cells. In the auditory nerve the number of (afferent) neurons is much bigger than the number of hair cells, because between 10 and 20 neurons have connection with one single inner hair cell. These neurons are called radial ‘type I’ and form the majority of neurons in the auditory nerve. Additional information about afferent innervation can be found in Ch. 3.3.1, Par.3 of this Textbook.
Besides of the afferent neural system there is an ‘efferent’ neural network in which information from higher auditory nuclei is sent down to more peripheral centers and finally to the cochlea. Whereas the functions of the efferent pathways from colliculus inferior and from cortex are unclear and unknown for a great deal, the anatomy and properties of the olivocochlear efferents, that connect the olivary complexes to the inner and outer hair cells, are well understood now. These efferents, called the olivocochlear acoustic reflex bundles, regulate the cochlear gain and frequency selectivity of the outer hair cells under acoustic stimulation.
The present chapter presents some striking examples of the reflexes (feedbacks) generated via the olivocochlear acoustic reflex bundles. Although this evidence is based on animal experiments, the scientific experience at this moment is enough far developed for extending the findings reliably to humans. Moreover several psychophysical experiments with efferent stimulation have been carried out already for humans (see e.g. Brashears et al., 2003). The topics here to be discussed aim to present a combined insight into the generation of the reflexes on the basis of the anatomic connections and into the way they influence the gain and frequency selectivity of the outer hair cells
These topics have been selected too because they are a further step in understanding auditory mechanisms like the detection of signals in noise and the protection of hearing against damaging high sound levels. This choice is in line with the aims of the Dutch Textbook of Audiology.
Subjects to be discussed:
- The anatomy of the olivocochlear acoustic reflex bundles (note that it not deals with the pathways responsible for the stapedius reflexes)
- The way in which, via these efferents, the cochlear gain and the frequency selectivity of the outer hair cells are regulated, both in quiet and in noise, and the potential function of these reflexes in protecting the auditory system against damage due to high sound levels.
The best known efferent pathways to the cochlea’s are the ‘olivocochlear reflex bundles’ (OCB), consisting of the medial olivocochlear (MOC) bundles (left and right) and the ‘lateral olivocochleaire (LOC) bundles (left and right). The medial bundles are connected with the outer hair cells (OHC) and the lateral ones with auditory-nerve fibers under the inner hair cells (IHC), as illustrated schematically in Fig.1. This is schematized from a transverse section of the brainstem and the right cochlea of the cat.
A second subdivision of this quartet is in two ‘crossed’ bundles (COCB), that start at the contralateral side (from the left in Fig.1) and two ‘uncrossed’ bundles (UOCB) starting at the ipsilateral side (at the right in Fig.1).
A third subdivision is in that in thin unmyealinated neurons and thick myelinated fibers. Note that in Fig.1 the thickness of the lines corresponds to the number of fibers in the bundles, not to the thickness of each fiber or the fiber’s myelination.
Fig.1. Schematical representation of the courses of the olivocochlear acoustic reflex bundles (OCB) to the right ear. De medial bundles haven been drawn in green and the lateral ones in red. The abbreviation COCB refers to crossed bundles and the abbreviation UOCB represents uncrossed bundles. The afferent bundle ascending from the inner hair cells to the (ventral) Cochlear Nucleus (CN), and farther on (see Fig.2) is indicated in black. The drawing is a transverse section of the brainstem. Illustration based on Fig.1 in Guinan JJ, 2006.
The connections in Fig.1 belong to the right cochlea. A similar, however, mirrored representation, is applicable to the left cochlea. For a complete picture this mirrored representation had to be placed upon that in Fig.1. Most anatomic connections originate from investigations of Warr (1978) and Warren & Liberman (1989).
The best investigated reflex is the contralateral MOC reflex (Fig.2). Sound presented to the right cochlea (at the right in this figure) causes excitation of afferente neurons from the inner hair cells (indicated in black). These afferents innervate reflex interneurons in the posteroventral part of the ipsilateral cochleaire nucleus (CN). These in turn innervate MOC neurons in the contralateral olivary complex which cross again (back) the brainstem and innervate the ipsilateral outer hair cells. Thus the ipsilateral reflex bundle crosses the brainstem twice.
Fig.2. Schematical representation of the generation of the ipsilateral reflex in the right ear via the crossed olivocochleaire (OCCB - MOC) bundle (green and thick). Illustration based on Fig.1 in Guinan JJ, 2006.
The contralateral reflexes in Fig.2 are evoked by stimulation of the left ear. In this case the afferent neurons run via the left cochlear nucleus to the (medial) MOC neurons in the ipsilateral (right) olivary nucleus (the dashed black line). From there the efferent neurons follow the thin green line at the right hand side in Fig.2, ending on the ipsilateral outer hair cells.
From a comparison of the thicknesses of the lines indicated in Fig.1 and Fig.2, which correspond approximately to the number of fibers involved, one might conclude that the ipsilateral reflexes are stronger than the contralateral ones. This conclusion is only applicable to animals, especially for the higher (basal) frequency regions. For humans so far no indications for such differences have been found. A possible reason for this might be the fact that the maximum sensitivity for sound is in a lower frequency region in humans than for the experimental animals investigated.
Direct contact of the MOC neurons with the outer hair cells occurs via the ‘Outer Spiral Bundle’ - OSB - Hfdst.3.2.2, Par.5). Also contacting outer hair cells are ‘type II’ afferent neurons. The dendrites of these afferents run into basal direction and thereby contact several outer hair cells. The efferente synapses are situated close to those of the afferente dendrites (see Fig.8 in Ch.3.3.1).
Activation of outer hair cells by efferent fibers regulates the gain of these cells at low stimulation levels. This ‘cochlear gain’, on its turn regulates the firing rates of the afferent neurons in the auditory nerve as illustrated schematically in Fig.3A. This has been demonstrated experimentally by presenting tone bursts to the ipsilateral ear of a cat and electrically stimulating MOC neurons at the contralateral side of the brainstem (Fig.2). The blue curve at the left represents the firing rates without MOC stimulation and the green curve is the result obtained with MOC stimulation. The decrease of gain in the middle of the dynamic range in this case amounts 20 dB. In general it is 10 to 25 dB, depending on the specific measuring position within the dynamic range. The cochlear gain and, thus, the decrease of it too are maximum at relatively low stimulation levels.
Fig.3.Schematic representation of the effects of electric stimulation of the contralateral medial olivocochlear bundle (MOC stimulation) on outer hair cell gain during ipsilateral acoustic stimulation with tone bursts in quiet, measured in cats:
A: Decrease of spike rate in an afferent single fiber in the auditory nerve ipsilaterally. Figure redrawn from Guinan JJ, 2006, Fig.5B.,
B: Increase of threshold in a tuning curve in the ipsilateral auditory nerve, especially at the characteristic frequency. Figure redrawn from Guinan JJ, 2006, Fig.4.
C: Reduction of amplitude of basilar membrane displacement in the ipsilateral cochlea. Redrawn from Russell and Murugasu, 1997, Fig.3D.
Decrease of gain, under MOC stimulation, is maximum at the characteristic frequencies of the fibers involved, as shown in Fig.3B. This is a ‘classical’ tuning curve of a single type I afferent neuron under two conditions, without MOC stimulation, having the well known sharp tip (blue), and the other one with MOC stimulation (green). 2. MOC inhibition reduces cochlear amplifier gain about 25 dB of the total of 50-60 dB. Note that MOC stimulation causes no shift in characteristic frequency. Finally, as expected now, MOC stimulation causes a reduction of the amplitude of basilar membrane displacement in the ipsilateral cochlea. (Fig.3C).
In the former section tone bursts in quiet were used in order to show the effect of MOC stimulation. With these stimuli electric stimulation of MOC neurons (at the contralateral side of the brainstem) reduced the firing rates of the afferent neurons from the ipsilateral cochlea. The opposite effect, an increase of firing rate ipsilaterally, occurs too under certain conditions. For transient stimuli, like tone bursts, presented to the right ear, now in a background of continuous noise, MOC stimulation causes an re-increase of firing rate in the afferent neurons. The effect is schematically shown in Fig.4.
Fig.4. Schematic representation of the effect of electric stimulation of the contralateral (crossed) medial olivocochleaire bundle (MOC stimulation) on the gain in the outer hair cells during ipsilateral stimulation with tone bursts in noise, measured in cats. The black curve (no noise and no MOC stimulation) is the same one as the one in Fig.3A. In case of the blue curve is continuous noise has been presented the right ear simultaneously with the tone bursts. The result is a reduction of the dynamic range of the fiber. The reduction is undone (‘unmasking’) under contralateral electric MOC stimulation (green curve). Figure redrawn from Guinan JJ, 2006, Fig.5D.
The black curve (no noise and no MOC stimulation) is the same as that in Fig.3A. In case of the blue curve continuous noise is presented to the right ear, simultaneously with the tone bursts. It results in a reduction of the dynamic range of the fiber. Probably, now the neural transmitter is partly used by the noise and therefore not available for the production of a sufficient high spike rate at high level tone burst. The reduction is undone (‘unmasking’) under contralateral electric MOC stimulation (green curve). It means that the transmitter is re-available for use, restoring the situation ‘as it was’, besides of the higher tone threshold. See also Ch.6.2.2, Fig.9.
Good insight in the effects of the olivocochleair efferents on otoacoustic emissions is obtained from several experiments carried out by Liberman et al. (1996). We describe one of them with the help of Fig.5A and Fig.5B. Fig.5B is a replica of Fig.2, added for better understanding the difference between the three conditions in Fig.5A. We here stress again that effects on otoacoustic emissions mean effects on the cochlear gain in the outer hair cells.
Fig.5A schematically illustrates three times the DPOAE amplitude in a cat in the ipsilateral (right) ear, generated by the primary tones f1 and f2 , with f2 = 4 kHz en f2/f1 = 1.2. The tones are turned on at time 0 and are presented during 10 seconds. From 3 seconds after the beginning, a broadband noise is presented to the contralateral ear during an interval indicated by the black bar. The sound level of the noise was 80 dB SPL. Middle ear muscles were cut.
Fig.5. Schematic representation of the effects of acoustic stimulation of the contralateral (left) ear on the size of the DPEAO in the ipsilateral (right) ear of a cat, before and after cutting the medial olivocochlear bundle at two places, respectively. The contralateral stimulus is a broadband noise with a sound level of 80 dB SPL. In case of the red curve all bundles are intact. The blue curve represents the situation with the crossed bundle (COCB) cut and the green curve the cutting of the whole olivocochlear bundle (OCB). Middle ear muscles were cut in all cases. The illustration at the right is the same one as that in Fig.2 and has been added for better understanding the one at the left. Figure at the left redrawn from Guinan JJ, 2006, Fig.7 en Liberman et al., 1996, Fig.6A.
When the uncrossed bundles (UOCB) and crossed bundles (OCB) are intact the DPOAE amplitude in the right ear follows the red curve. The curve is characterized by a fast decrease (adaptation) at the beginning and again a fast decrease when the contralateral noise is turned on. As soon as the noise turned off the DPOAE returns to its original value.
When the crossed bundle (COCB) is cut (thus at the contralateral side - left - in Fig.5B) the fast adaptation in the beginning disappears, resulting in a less sensitive starting position of the DPOAE amplitude in Fig.5A (blue curve). It is highly probable that this fast adaptation reflects the ipsilateral (right ear) acoustic MOC reflex. This effect crosses the brainstem twice, firstly via the afferents to the contralateral medial olivary complex and subsequently back, along the efferent MOC bundle to the ipsilateral outer hair cells. Contrary the effect of the noise in the left ear on the amplitude remains, because this activates the medial bundle at the right (ipsilateral) side which reduces the cochlear gain in the outer hair cells of the right ear.
De green curve is found when the whole olivocochlear bundle has been cut, e.g. at the right hand side in Fig.5, where the four sub bundles go together (OCB). In this case both the decrease due to the contralateral noise and the fast adaptation at the beginning are absent, the latter already being absent in the blue curve
As already mentioned these highly interesting experimental results are fully in line with the anatomy of the olivocochlear bundles: the ipsilateral acoustic reflex (MOC) going via the contralateral pathway (vice versa) and the contralateral reflex going from the contralateral side to the ipsilateral one.
The decrease of cochlear gain in outer hair cells under MOC stimulation might have a function in protecting the cochlea against damage due to high sound levels. An illustration of such a protection is the effect of MOC stimulation on the size of the temporary threshold shift (TTS) induced by high level sounds in guinea pigs, as investigated by Rajan (1988a,b) and Rajan end Johnstone (1988). Some results of their experiments are described now. Fig.6 presents a schematical illustration of them.
The red triangle in Fig.6A shows the mean TTS that is present in guinea pigs after they have heard a 10 kHz tone of 103 dB SPL to one ear during 1 minute. The threshold was measured by means of the N1 of the Compound Action Potential (CAP), starting 5 minutes after the end of the traumatizing sound. The TTS is maximum at a frequency of 14 kHz (this is a usual value) and amounts 22 dB. When, simultaneously with the conditioning sound, the COCB is stimulated electrically (MOC stimulation, thus at the contralateral side) the TTS is much less (10 dB, the green triangle).
Fig.6. CAP thresholds (N1) in guinea pigs as a function of frequency as a result of TTS, elicited by traumatizing the right ear the animal with a 10 kHz tone of 103 dB SPL during 1 minute The measurement of the thresholds was started 5 minutes after the end of the traumatizing sound. The red triangles, both in Fig.6A and Fig.6B represent the results for unprotected situations. The green triangles illustrate the effects of efferent stimulation (simultaneously with the traumatizing sound), either electrically (Fig.6A) or acoustically (Fig.6B) on the size of the TTS.
Fig.6A. Decrease of TTS after simultaneous contralateral electric (MOC) stimulation (COCB intact). Fig.6B. Decrease of TTS after simultaneous acoustic stimulation of the contralateral ear with noise (COCB intact). The black triangle in Fig.6B represents the effect van simultaneous acoustic stimulation of the contralateral ear with noise after cutting the COCB.
Fig. 6A: Schematically redrawn from Fig.1B in Rajan, 1988b
Fig.6B: Schematically redrawn from Fig.5A in Rajan and Johnstone, 1988
De different triangles refer to different groups of guinea pigs.
If the COCB has been cut on beforehand, contralateral stimulation yields no protection. Then the CAP thresholds are similar to the case in which the COCB is intact and the contralateral stimulus is absent (red triangle in Fig.6B).
The mechanisms responsible for the influencing of the cochlear gain in the outer hair cells and the role of the neurotransmitters are not discussed in this textbook. This topic is too specialistic for it.
This chapter describes some experiments that are illustrative for the way in which olivocochlear efferents modulate the cochlear gain of the outer hair cells. The effects are:
- Influence on cochlear gain in the outer hair cells under stimulation with tone bursts by means of electric stimulation of the olivocochlear efferents (olivocochlear bundle) at the contralateral side
- Decrease of reduction (‘unmasking’) in dynamic range under stimulation with tone bursts in noise after electric stimulation of the olivocochlear bundle at the contralateral side (‘unmasking’ - improvement of signal to noise ratio)
- Effect on DPOAE’s by electric stimulation of (contralateral) MOC efferents and by noise presented to the contralateral ear
- Decrease of temporary threshold shift (TTS) under electric (MOC) and acoustic stimulation of the olivocochlear efferents at the contralateral side of the traumatized ear.
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