So now to The Ear. Drawings from Max Brodel, an Austrian artist who came to Johns Hopkins in the 1920s. My point in showing this figure is to
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1 So now to The Ear. Drawings from Max Brodel, an Austrian artist who came to Johns Hopkins in the 1920s. My point in showing this figure is to emphasize the intricate and well-protected structure of the inner ear, encased in the temporal bone. This combination of fragility and inaccessibility is a large part of the explanation for why knowledge of hearing has somewhat lagged others, such as the vision and olfaction. 1
2 What does it mean to analyze the frequency components of a sound? A spectrogram such as that shown here is the usual display of frequency components as a function of time here during the production of a sentence I can see you. We will see a real-time spectrograph in operation ourselves. 2
3 Today I will provide an overview of cochlear function. Sound enters the external ear, initiating motion of the eardrum and attached ossicular chain, resulting in fluid movement within the inner ear, in the cochlea. 3
4 Structure and Function of the Auditory and Vestibular System - 1 Schematic representation of externally recorded electrical cochlear response waveforms and their relations to each other. The stimulus consists of two bursts lasting about 18 ms. The second tone burst is inverted in polarity with respect to the first. From the bottom up, the cochlear microphonic response CM exactly follows both stimulus waveforms. The summating potential SP is by definition non oscillatory and follows the envelope of the stimulus. The compound or whole nerve action potential CAP is present only at the start and end of stimulation. The top trace shows the composite electrical signal as it would actually be recorded. The CM, SP and CAP traces are simply added. The composite responses to the two stimuli are different only because of the polarity inversion of CM. Subtraction of the two composite waveforms would leave only the CM trace, whereas adding them together would eliminate CM and leave the sum of SP and CAP traces. (From D.T. Kemp, Otoacoustic emissions and evoked potentials, in The Ear, volume 1 of the Oxford University Press Handbook of Auditory Sciences, (P. Fuchs, ed.) to be published in 2010.) 4
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6 Motion of the stapes footplate causes fluid motion, resulting in deflection of the cochlear partition upon which are situated the hair cells and surrounding supporting cells. Frequency selectivity begins with the fact that the mechanics of the cochlear duct vary from end to end. Consequently, lower frequency tones cause maximal vibration at positions near the cochlear apex. High frequency tones deflect the stiffer partition nearer the oval window. This tonotopic pattern of vibration was described first by von Bekesy and is the basis of frequency selectivity in the mammalian cochlea. 6
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8 The tonotopic organization of the cochlea, and the selective innervation of that sensory epithelium, is taken advantage of with the cochlear implant. For the profoundly deaf, a set of electrodes are threaded into the cochlea. A spectrum analyzer provides frequency-dependent stimulation to each electrode, which then stimulates the nearest auditory nerve fibers. With practice this very limited input (usually ~ 10 working electrodes) can be used to understand speech. The best success has been obtained in post-lingually deafened adults, and in congenitally-deaf children who receive the implant in the first year or two of life. In the best cases otherwise deaf children can hit age-appropriate educational milestones. 8
9 Structure and Function of the Auditory and Vestibular System - 1 Example of the human cochlea obtained from a 5 month old fetus. The coil provides a continuous pathway for sound wave propagation. The stapes footplate moves into and out of the oval window (blue arrow), driving fluid motion that is relieved (at steady-state) at the round window (yellow arrow). 9
10 Structure and Function of the Auditory and Vestibular System - 1 Components of the membranous labyrinth 10
11 Structure and Function of the Auditory and Vestibular System - 1 We have already noted the two types of cochlear fluids, perilymph and endolymph, and how separate portions of the hair cells (in fact, ALL hair cells) are exposed to these solutions. Perilymph is similar to most extracellular fluids (e.g. CSF), being high in Na and low in K. Recall that this solution bathes the basolateral surface of hair cells (i.e. the barrier to endolymph is the reticular lamina, not the basilar membrane). Endolymph is a highly unusual extracellular fluid, being high in K, low in Na, and very low in Ca. This is very similar to most intracellular environments, where potassium is the dominant ion. Thus, the transduction current into hair cells is largely a potassium current. But without a concentration gradient, there must be another driving force to get potassium into the cell. This driving force is generated by two electrical potentials. First, the hair cell s resting potential is ~ -60 mv due to ion channels in the basolateral portion of the membrane. Second, there exists an endolymphatic potential that is +80 mv with respect to the vascular system. This so-called endocochlear potential combines with the hair cell s resting potential for an ~140 mv driving force pushing potassium into the hair cell. The source of the endocochlear potential remains unclear, though it is intimately tied to the stria vascularis which secretes potassium into the endolymphatic space. It should be noted that the endocochlear potential itself is not necessary to proper hair cell function since this potential is only a few mv in the vestibular system (and virtually absent in non-mammalian inner ears). Yet, if the stria is damaged or the endocochlear potential is eliminated, auditory sensitivity is reduced. It may be that the high frequency environment of the cochlea and voltage-dependent motility of some hair cells benefit from the added push of the endocochlear potential. (right slide image: adapted from Promenade, S. Blatrix) 11
12 Structure and Function of the Auditory and Vestibular System - 1 The recycling of potassium and the homeostasis of endolymph is of particular interest, since a stable ionic environment is critical for proper hair cell function. The endolymphatic compartments of each inner ear organ and a separate endolymphatic sack are contiguous. While some secretion and resorption of potassium may occur by the flow of endolymph through this network, there is strong evidence that the recycling of potassium is under local control. The illustrations above depict current theories, where potassium is secreted by the stria, taken up by hair cells in transduction, released from the hair cell s basolateral surface, and recirculated to endolymph via a system of gap junctions between epithelial supporting cells and connective tissues at the spiral ligament. From the fibrocytes of the spiral ligament, potassium presumably enters the stria again by gap junctions. The combination of Na,K- ATPase and Na-K-Cl cotransporters in the marginal cells of the stria enable the accumulation of potassium in these cells (indeed they have a highly positive resting potential). Slowly gating potassium channels on the endolymph-facing surface of marginal cells leads to the accumulation of potassium in endolymph. Immunoreactivity supports connexins as likely components in this network of gap junctions. Mutation of the connexin 26 gene leads to non-syndromic sensorineural hearing loss and the loss of endolymphatic potential. 12
13 Outer hair cells are mechanically active. In response to a sound-induced change in membrane potential, they move. This movement of the outer hair cells adds to that of the cochlear membranes, and so enhances the stimulus energy delivered to the inner hair cell. So, outer hair cell damage deafens the cochlea and is a common form of hearing loss. 13
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18 Will describe results obtained by intracellular voltage-clamp recording from afferent dendrites at point of contact with IHCs. The peculiar advantages of this experiment provide new insights into ribbon function, and perhaps by extension, into mechanisms of transmitter release more generally. 18
19 Low frequency tones produce phase-locked activity in afferent fibers (turtle). 19
20 Temporal coding results from phase-locking, accurate to submillsecond. 20
21 At CF phase is independent of intensity. As sound gets louder, hair cell is more strongly depolarized, but spike initiation time does not vary. How does this occur, compare to other chemical synapses? 21
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25 This is what the mammalian cochlea (2-3 week old rat) really looks like. These are otic capsules, the bony chamber within the temporal bone of the skull that encloses the inner ear. On the right is the intact capsule. On the left the surgeon (Dr. E. Wersinger, PhD) has dissected away the surrounding bone to reveal the soft tissues of the cochlear spiral. 25
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28 The synaptic currents reverse in sign near 0 mv, so flow through non-selective cation channels. They are blocked by AMPA/kainate receptor bocker CNQX, and lengthened by cyclothiazide, indicating they are subserved by AMPA receptors. 28
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30 The mammalian cochlea possesses two classes of afferent neurons and two classes of efferent neurons. Type I afferents contact single inner hair cells to provide acoustic analysis as we know it. Type II afferents branch extensively to contact numerous outer hair cells. Medial efferent neurons synapse on outer hair cells. Lateral efferent neurons synapse on Type I afferents beneath inner hair cells. 30
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33 I increase the likelihood of recording from a Type II fiber by recording at an age P5-P9 when efferents have not fully innervated the OHC region in rats. Examining the morphology of the labeled fibers gives confirmation that I am recording from Type II s, as the morphology of these cells has been very well described. This image shown a confocal stack of a fiber that I have recorded from and filled with a tracer, in green. The large blob is artifact, due to blowing some of the dye around the recording region. On the left is a tracing of a filled fiber from another recording showing the classic radial projection from the filled soma and a right hand turn towards the base of the cochlea. I should note that I have only observed a soma recording in this one filled neuron. 33
34 We have also determined that the EPSC s are glutamatergic. This figure shows the average EPSC waveform for synaptic events that occur when the membrane holding potential is held at the voltages shown here. Graphing the average peak amplitude of the events by the membrane holding potential illustrates that the currents reverse polarity at a holding potential of 0mV, which is consistent with conductance through a non-selective cation channel. Additionally, the EPSC s are eliminated by the AMPA receptor blocker NBQX at 10uM as seen in the trace on the left. The amplitude by diary plot shown on the right shows the complete blockage of synaptic events upon NBQX application, followed by their return upon washing off the drug. 34
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39 The mammalian cochlea possesses two classes of afferent neurons and two classes of efferent neurons. Type I afferents contact single inner hair cells to provide acoustic analysis as we know it. Type II afferents branch extensively to contact numerous outer hair cells. Medial efferent neurons synapse on outer hair cells. Lateral efferent neurons synapse on Type I afferents beneath inner hair cells. 39
40 Idealized vibration pattern of the basilar membrane (cochlear partition on which hair cells reside). Passive mechanism refers to the vibration pattern produced by a pure tone in a dead cochlea (or one without outer hair cells). Active mechanism refers to the pattern of vibration in a healthy, live cochlea, made 50 db more sensitive and much more sharply-tuned by the active mechanical contribution ( electromotility ) of outer hair cells. 40
41 Outer hair cells are mechanically active. In response to a sound-induced change in membrane potential, they move. This movement of the outer hair cells adds to that of the cochlear membranes, and so enhances the stimulus energy delivered to the inner hair cell. So, outer hair cell damage deafens the cochlea and is a common form of hearing loss. 41
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44 Oto-acoustic emissions are ear sounds due to active motility of outer hair cells. They are an indication of normal cochlear function. Typically recorded as the distortion product (2f1-f2) produced by two tones (f1, f2) presented simultaneously to the ear. A sensitive microphone in the ear canal is the detector. 44
45 Otoacoustic emissions are a useful clinical tool, enabling tests for cochlear health in prelingual, or otherwise uncommunicative patients. 45
46 Spontaneous otoacoustic emissions in a newborn. 46
47 47
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