Hearing Impairment 2
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1 Hearing Impairment 2 Zdebik AA, Wangemann P, & Jentsch TJ (2009). Potassium ion movement in the inner ear: Insights from genetic disease and mouse models. Physiology, 24, Kujawa SG, Liberman MC (2009). Adding Insult to Injury: Cochlear Nerve Degeneration after Temporary Noise-Induced Hearing Loss. J. Neurosci 29: (2009). Schmiedt RA, Lang H, Okamura H, Schulte BA Effects of furosemide applied chronically to the round window: A model of metabolic presbyacusis. J. Neurosci 22: (2002). Zeng FG, Kong YY, Michalewski HJ, Starr A (2005). Perceptual consequences of disrupted auditory nerve activity. J Neurophysiol 93: Cai S, Ma W-LD, Young ED (2009) Encoding intensity in VCN following acoustic trauma: Implications for loudness recruitment. JARO 10:5-22. Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, Liberman MC (2010). Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30: The most common genetic cause of deafness is a mutation in the connexin 26 gene (DNFB1), which codes for a gap junction channel. This suggests that the potassium recycling system of the cochlea is damaged, the red arrows marked 1. 1
2 Largely on the basis of anatomical evidence, it has been suggested that potassium recycling occurs by a complex intracellular pathway through supporting cells and fibrocytes in the walls of the scala media and the spiral limbus. Spicer and Schulte, 1998 Spicer and Schulte caption: A schematic representation of the proposed medial and lateral! transcellular routes for dispersal and conservation of K + effluxed from inner and outer hair cells during auditory transduction. Ions released from inner hair cells (IH) diffuse medially through border cells (BP), inner sulcus cells (IS) and lateral interdental cell (LI) columns to the undersurface of the tectorial membrane and from ISCs through stellate fibrocytes (SF) to capillaries (Cap) or to central interdental cells (CI) and the scala media. K + pumped from scala vestibuli into supralimbal cells (SL) flows downgradient to light fibrocytes (LF) and medial interdental cells (MI) for return to scala media.! In the lateral route, K + fluxing from outer hair cells (OH) is resorbed by Deiters (D) and tectal cells (T) and flows via gap junctions through Hensen (H), Claudius (C), and outer sulcus cells (OS) and their root processes (RP) to flux into stroma maintained at a low K + level by the Na,K-ATPase activity of type II fibrocytes. K + subsequently diffuses via gap junctions through type I fibrocytes (Ia,Ib) and strial basal (B) and intermediate cells (I) into the intrastrial compartment kept low in K + by the pumping activity of strial marginal cells (M). K + resorbed by type V fibrocytes from scala vestibuli diffuses downhill through Ib then Ia fibrocytes to the stria. B=basal cell; BP=border cell; Cap=capillary; C=Claudius cell; CI =central interdental cell; D=Deiters cell; H=Hensen cell; I=intermediate cell; IH=inner hair cell; IS=inner sulcus cell; M=marginal cell; MI=medial interdental cell; LF =light fibrocyte; LI=lateral interdental cell; OH=outer hair cell; OS=outer sulcus cell; RP=root process; SF =stellate fibrocyte; SL=supralimbal fibrocyte; T=tectal cell; Ia, Ib, II, IV, and V=types of lateral wall fibrocytes. 2
3 The current concept of endolymph production involves potassium transport through a multicellular system in the stria vascularis. The energy for production of the high K + concentration in endolymph and the EP is the Na-K ATPase in the strial marginal cells. The rest of the K + transport steps are thought to be passive. Note that the source of potassium is thought to be intracellular in fibrocytes of the lateral wall. Mutations of KCNQ1 and KCNJ10 are deafness genes, and knockouts of SLC12A2 (the Na-2Cl-K cotransporter) lead to a collapse of the endolymphatic space, suggesting no endolymph production. Also mutations of the tight junctions (claudin 11) between basal cells reduces the EP. Wangemann, 2002 A compartmental model showing the potassium recycling system. Transport is all passive except for the two active transports. Endolymphatic space: High K + Low Na + and Ca mv potential Perilymph space: Low K + High Na + 0 potential Kikuchi et al
4 Immunocytochemical evidence for the location of the relevant transporter systems from the model (mouse cochlea). Note the localization of the transporters as postulated in the model on the previous slide. Note also the distribution of connexin 26 along most of the pathway. H & E Na-K ATPase Na-K-Cl 2 xporter Connexin 26 Kikuchi et al An evidence that favors the intracellular K + recycling pathway is that one of the most common deafness genes ( 25% of cases) is connexin (DFNB1). Connexins form gap junctions, which are non-selective ion channels that directly connect the interiors of cells. Connexins are found in the supporting cells and fibrocytes of the cochlea. They appear about the same time that the EP develops and are thought to provide the intracellular route for K+ recycling. Kikuchi et al
5 The connection of presbyacusis to degeneration of the stria-vascularis/ep/endolymph system was provided by Schmiedt, Schulte, Mills, and colleagues. In aging (3 yrs old) gerbils that are not exposed to noise, hearing degenerates but hair cells are reasonably normal. The largest change is a reduction in the EP (from mv in young animals to mv in aged animals). It is the EP change that matters because the K + concentration is normal in the aged animals. Sewell has shown that EP reduction lowers the spontaneous activity of auditory-nerve fibers (-0.02 log units of rate/mv) and increases the threshold (0.9 db/mv), presumably by reducing the electrochemical potential driving transducer currents into hair cells. Support for the connection between loss of EP and loss of hearing in aged animals is provided by the fact that a similar hearing loss can be produced by furosemide treatment of the cochlea in young animals. Furosemide blocks the Na/2Cl/K cotransporter and reduces the EP, presumably without affecting hair cells or transduction. Schmiedt et al.,
6 Recent attention has shifted away from hearing impairment attributable to cochlear transduction, toward effects on the auditory nerve and circuits in the central nervous system. After recovery from an acoustic trauma that does not destroy hair cells, auditory nerve fiber synapses disappear from the hair cells. Much later (64 weeks below) spiral ganglion cells degenerate. There is evidence that this is an excitotoxic effect, damage to nerve fibers by excessive glutamate released from hair cells during the trauma. Kujawa and Liberman
7 The loss of AN terminals and eventually spiral ganglion cells causes a decrease in the amplitude of the ABR (central neuron responses), even though DPOAEs (OHC) recover from the trauma. TTS TTS Note that the DPOAE recovers, whereas the ABR does not. HOWEVER, the ABR threshold does not change. This fact has important implications for auditory testing, which frequently emphasizes thresholds rather than suprathreshold amplitudes. Kujawa and Liberman 2009 A long decline in spiral ganglion cell numbers is observed in human temporal bones. This occurs uniformly along the cochlea and is not obviously associated with a pathological process. Makary et al
8 The properties of either cochlear or auditory nerve degeneration do not seem to match the properties of auditory neuropathy. Neuropathy seems to affect temporal measures of auditory perception such as pitch discrimination at low frequencies temporal integration temporal modulation detection gap detection backward and forward masking signal detection in noise binaural beats interaural time differences. It has less effect on intensity-related perception, such as loudness discrimination, pitch discrimination at high frequencies, and sound localization using interaural level differences. The distribution of effects of cochlear or auditory nerve degeneration are more or less the opposite. (Zeng et al. J Neurophysiol 93: , 2005.) One possible animal model for neuropathy is the bassoon mutant, a mouse which is missing an essential component of the hair-cell synaptic ribbon. This seems to lead to a temporal disordering of some aspects of auditory nerve responses. The DPOAEs are normal, whereas the ABR threshold is substantially elevated Most aspects of auditory-nerve spike trains are normal, including phase locking, except that first-spike latencies are quite sloppy. ABRs Buran et al
9 Loudness recruitment is a prominent feature of hearing impairment. Recruitment means the growth of loudness is steepened (left plot).! To explain this, note that the responses of the BM response become steeper in impaired ears (right plot), but...!?!?! Buus and Florintine 2002! Ruggero et al. 1997!... if cochlear responses are the explanation for recruitment, then the growth of response in the auditory nerve fibers would also be steeper. In fact, it is the same or somewhat less steep.!?! Heinz and Young 2004! 9
10 ... if cochlear responses are the explanation for recruitment, then the growth of response in the auditory nerve fibers would also be steeper. In fact, it is the same or somewhat less steep.! X!?! (histograms of the slope measurements of ANFs)! Heinz and Young 2004! Loudness is probably determined by the summated activity of groups of auditory neurons, not by single neurons.! frequency! 10
11 To enable a comparison of psychophysical and physiological data, use binaural loudness balance.! A listener with one impaired ear equates the loudness of sounds between the better and the impaired ear. Recruitment is clear in such subjects:! If the two ears are both good (or equally bad) then the data should lie on the lines with slope 1.! The steep slope of these curves shows that loudness grows faster in the impaired ear.! Stillman et al. 1993! Auditory nerve fibers do not show recruitment when analyzed with loudness balance. The assumption here is that equal summated rates should correspond to equal loudness! X!?! Summated rate! Rate balance! The expected behavior!! Actual neural balances have slopes <1.! Heinz, Issa, Young 2006! 11
12 Cell types in ventral cochlear nucleus differ in the way auditory nerve inputs are integrated in their dendrites.! bushy multipolar After Osen and Roth 1969; Sento and Ryugo 1989; Ostapoff et al. 1994; Wu and Oertel 1984; Ferragamo et al ! Recruitment seems to occur at the first synapse in some neurons in the central auditory system.! Bushy and multipolar neurons change their rate responses in opposite ways following acoustic trauma.! bushy X!!! multipolar X! Cai, Ma, Young 2009! 12
13 The neural loudness balances correspond exactly to behavioral results for the multipolar population, but not the bushy population.! Thus an important component of recruitment seems to occur in the cochlear nucleus and not in the cochlea.!!! X! bushy multipolar Cai, Ma, Young 2008! Following moderate acoustic trauma, degeneration and formation of new synaptic terminals is seen in the cochlear nucleus for up to 32 weeks. There is a tendency for a shift toward more excitatory versus inhibitory terminals. 4 khz octave noise band, 3 hrs, 108 db. There is substantial OHC loss and mild nerve-fiber and IHC loss. Kim, Gross, Morest, Potashner
14 Neurons generally receive a mixture of excitatory and inhibitory inputs and show corresponding responses to sound.! DCN! Cochlea! Inf. collic.! Auditory nerve! sound level! frequency! Spirou and Young 1991! Following moderate acoustic trauma (~50 db), inhibitory responses of neurons are reduced. The examples below are from the dorsal cochlear nucleus. Presumably, this changes the signal-processing function of such neurons.! Cochlea Inf. collic. Aud. nerve Normal! Trauma! Note broadly tuned responses with little inhibition.! Ma and Young 2006! 14
15 Plasticity in the connections from cochlea to the inferior colliculus (IC): the mapping from cochlea to the inferior IC can be demonstrated by electrically stimulating a point in the cochlea and measuring the thresholds of IC neurons. If done in an acute preparation, the tuning is consistent with point-to-point connections. CI stimulation Neuron recording inferior colliculus Leake et al, 2000 The location of the responsive neurons moves with the site of stimulation in the cochlea. CI stimulation Neuron recording inferior colliculus Leake et al,
16 If stimulation is done chronically for a few weeks, the precision of the mapping decreases, suggesting a reorganization of the anatomical connections that decreases the precision of the tonotopic pattern. acute CI stimulation Neuron recording chronic inferior colliculus Leake et al, 2000 Moving the stimulation site again moves the response pattern in the inferior colliculus, but the representation is again broadened. CI stimulation Neuron recording acute chronic inferior colliculus Leake et al,
17 Presumably the damage is done by the misapplication of plasticity that connects neurons activated by the same or similar stimuli. Ordinarily this form of plasticity (Hebbian) organizes neural circuits. The problem in this situation is that the electrical stimulation activates much of the whole auditory nerve simultaneously, not a natural, tonotopic pattern. Thus the inappropriate plasticity. Note that with moderate hearing impairment, natural acoustic stimulation produces a similar widespread activation pattern in the auditory nerve. Central degenerative processes may continue throughout the auditory system, even up to the cortex. The plasticity may be subject to modification by the acoustic environment. The data show maps of the tonotopic organization of auditory cortex before (A) and after (B,C) a mild acoustic trauma (20-40 db threshold shift). A B C Following acoustic trauma, Group 1 was untreated but Group 2 was exposed to moderate-level complex stimuli designed to produce activity in the damaged region of the cochlea. The tonotopic map of cortex was maintained.! Noreña & Eggermont
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