The mammalian cochlea possesses two classes of afferent neurons and two classes of efferent neurons.
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3 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. 3
4 Type I afferents contact single inner hair cells and make up 95% of the VIIIth nerve. The main (only?) source of acoustic information to the brain. Type II afferent contact many outer hair cells. Not known what information they carry to the brain, although it is suspected they may only be activated during very loud sound. 4
5 Will describe results obtained by intracellular voltage clamp recording from afferent dendrites at point of contact with IHCs. The particular advantages of this experiment provide new insights into ribbon function, and perhaps by extension, into mechanisms of transmitter release more generally. 5
6 Low frequency tones produce phase locked activity in afferent fibers (turtle). 6
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9 Synaptic proteins of hair cells differ from those at phasic synapses in CNS and elsewhere. 9
10 The protein ribeye makes up 70% of the molecular mass of the dense body. Molecular tethers (~30 nm in length) tie vesicles to the dense body of the ribbon. The protein bassoon might serve to anchor the ribbon to the plasma membrane. Otoferlin may serve as the hair cell s synaptotagmin (calcium sensor for vesicular fusion). Voltage gated calcium channels (CaV1.3) cluster near ribbon. 10
11 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. 11
12 Postsynaptic recordings to study transmitter release. 12
13 Spontaneous release from ribbon synapses occurs at low frequency in immature hair cells (before hearing onset at P12). These events are seen as transient inward currents at a negative membrane potential ( 94 mv). 13
14 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. 14
15 Seen at higher temporal resolution, the majority of synaptic events have classic alpha shape with a rapid rise and slower fall. At room temperature these in a fraction of a ms, and fall with a time constant of 1 ms. 15
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19 A frequency sweep stimulus was used to determine the selectivity and sensitivity of a single auditory nerve fiber. Action potentials (vertical ticks) occur at a particular time point, corresponding to a particular frequency during the sweep. The characteristic frequency (cf) is that which elicits action potentials at the lowest intensity. As intensity rises action potentials are driven by a wider and wider band of frequencies. 19
20 Tuning curves are derived from the sound pressure (intensity) necessary to produce a threshold response in the afferent fiber. Thus, at the characteristic, or best frequency, the fiber is most sensitive but louder sounds are required to elicit the same response at lower and higher frequencies. Sharp tuning means a narrow V shaped tuning curve. 20
21 The entire acoustic frequency range is represented among the population of afferent fibers innervating the cochlea. 21
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23 Upper panel: synaptic potentials and action potentials occur spontaneously (in the absence of sound) in a turtle auditory afferent neuron. A time histogram of action potentials shows that these occur at time intervals corresponding to the acoustic waveform phase locking. Note that the negative phase reduces firing probability below the spontaneous level. This is observed generally in auditory afferents of many species. Spontaneous activity (in the absence of sound) is modulated into phase with an acoustic stimulus. Note also that this modulation is biphasic: above average rate in one phase, below average rate in the opposite phase. This is one of the lines of evidence that tells us hair cells are partially activated at rest. The off direction of hair bundle movement hyperpolarizes the cell, reducing transmitter release. Therefore, at rest some MET channels must be open and partially depolarizing the cell. 23
24 Temporal coding results from phase locking, accurate to submillsecond. 24
25 At low frequencies (below ~ 5 khz), afferent neuron action potentials tend to occur in phase with the acoustic stimulus. At higher frequencies phase locking fails and action potentials have random timing. With louder sounds the number of action potentials per stimulus increases i.e., intensity is coded by firing frequency. However, note that action potential also can encode low sound frequencies by timing (phase locking). For louder sounds afferent firing shows adaptation a gradual decline in firing frequency (only evident in figure for higher frequency stimulus). Adaptation results from a decline in the number of vesicles available for release from the ribbon. 25
26 Membrane time constant = ~1 ms (determined by the product R m C m ), confers a low pass filter onto receptor potentials, with the corner frequency (where amplitude falls 50%), f 3dB = 1/2 is approximately 1600 Hz (in this example). As gets shorter (for example in smaller cells with smaller C m, or by increasing the # of channels open in the membrane to reduce R m ), then the corner extends to higher frequencies. N.B. inner hair cells (connected to afferent neurons) have longer membrane time constants than do outer hair cells (where electromotility happens). Inner hair cells do not vary as significantly in size and electrical properties as do outer hair cells along the tonotopic axis. 26
27 Adaptation of afferent firing during sustained tone can be attributed to depletion of a readily releasable pool of synaptic vesicles at the ribbon. 27
28 You see at a the beginning of the pulse (and in the extrended trace) an EPSC is activated in the first ms and then the rate drops to about 0.2 EPSCs per ms. Here you see the deconvolved afferent response. In comparison, this plot shows the rate of APs in response to a tone burst, a typical auditory nerve fiber response showing adaptation in the auditory nerve. As has been suggested before, we conclude that synaptic depression and the exhaustion of vesicles could account for adaptation in the auditory nerve. 28
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30 As sound intensity rises, firing rate of auditory afferents increases. The resulting intensity response curve has a threshold, a maximum slope, and usually saturates for loud sounds. Among cochlear afferents some have high spontaneous rates, low thresholds and narrow dynamic range ( hi spont fibers). Lo spont fibers have higher thresholds, lower slopes, and sloping saturation. Hi spont and low spont afferents can be connected to the same inner hair cell, requiring that some aspect of transmitter release varies between different ribbons in a single hair cell. 30
31 Low spont fibers are smaller and tend to innervate the side of the inner hair cell closer to the spiral ganglion (modiolus). High spont fibers are bigger and tend to innervate the inner hair cell on the side furthest from the ganglion (pillar). 31
32 Inner hair cells are isopotential so receptor potential identical at all ribbon synapses. Current studies suggest that the number of voltage gated calcium channels may vary between ribbons, conferring different release probabilities. Also, postsynaptic threshold, input resistance, modulation by lateral efferents may vary between different afferents. 32
33 Individual type 1 afferents that contact one inner hair cell can differ in their spontaneous rate, acoustic threshold and dynamic range. How can this be? The inner hair cell is isopotential, that is, the membrane potential is identical throughout. So every synapse is subject to the same voltage changes. And yet, some fibers have high spont rates, other fibers on the same cell have much lower spont rates. One idea for which some evidence is accumulating is that the number of voltage-gated calcium channels may differ between different active zones (ribbons). 33
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35 Afferent dendrites can be damaged and retract after excessive stimulation: glutamate toxicity. Mechanism thought to involve calcium-loading that activates calcium-dependent proteases to dissolve cytoplasmic structure. 35
36 36
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