Download The Auditory Pathway: Transmission between Hair Cells and Eighth

Auditory and Vestibular Sensation 463
The BK channels in hair cells of frogs,39 turtles,40 and chickens41,42 are encoded by a gene
whose mRNA is subject to alternative splicing of its composite exons. Some differentially
spliced isoforms of the channel are kinetically distinct.43 Additional variability may be
provided by an accessory β-subunit that combines with the channel and slows its gating
kinetics.44 Although BK channels also are expressed in the mammalian cochlea, there is
little alternative splicing,45 and no evidence for electrical resonance in inner or outer hair
cells. Nonetheless, as in birds,46 BK channels appear in rodent cochlear hair cells near the
onset of hearing47 and are more numerous in higher-frequency hair cells.48,49 The expression of mRNA significantly precedes that of functional channels, and developmental and
tonotopic expression patterns appear to be regulated at the level of membrane localization
of protein.50,51
The Auditory Pathway: Transmission between
Hair Cells and Eighth Nerve Fibers
Depolarizing and hyperpolarizing receptor potentials alter the open probability of voltagegated calcium channels in the hair cell’s basolateral membrane. Calcium entry in turn alters
the rate of release of neurotransmitter (glutamate) onto the terminal of a postsynaptic
afferent neuron. Hair cells, like retinal photoreceptors and bipolar cells, employ so-called
ribbon synapses for tonic transmitter release52 (Figure 22.11; see also Chapters 13 and
20). Even in the absence of a stimulus, the membrane potential of the hair cell is positive
to the threshold for gating of voltage-activated calcium channels; consequently, release
of glutamate is ongoing and excites the afferent fibers, giving rise to spontaneous action
potentials. At frequencies below ~5 kHz, the sinusoidal receptor potential in cochlear hair
cells alternately increases and decreases the rate of transmitter release, producing phaselocking in the postsynaptic firing pattern. At frequencies greater than 5 kHz, the hair cell’s
membrane time constant prevents rapid changes in membrane potential and the resulting
afferent activity simply increases above the spontaneous rate for the duration of the tone,
without cycle-by-cycle phase locking.
A type I afferent neuron in the mammalian cochlea has a single dendrite that is postsynaptic to a single ribbon in a single inner hair cell.53 Afferent action potential activity
often exceeds 100 Hz, requiring that the ribbon synapse have an impressive capacity to
marshal and release vesicles.54–56 Given that each inner hair cell ribbon tethers only 100–200
vesicles,57 it is still mysterious how this occurs. A further surprise is that spontaneous
(A)
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(B)
Displacement
Period
Amplitude
FIGURE 22.11 Hair Cell to Afferent Signaling (A) Type I spiral ganglion neurons are postsynaptic to single ribbon synapses of a single inner hair cell. The ribbon synapse has an electrondense core to which are tethered ~100 synaptic vesicles. Sinusoidal stimulation of the hair cell
gives rise to phase-locked activity in afferent neurons. (B) Individual afferent fibers contacting a
single inner hair cell can have different firing rates, both spontaneous and evoked.
©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
464 Chapter 22
transmitter release from ribbon synapses appears to be multivesicular; that is, it can be
composed of several vesicles released simultaneously.58 It is likely that ribbon function may
involve unique proteins differing from those serving release at other chemical synapses.59,60
58
Glowatzki, E., and Fuchs, P. A. 2002. Nat.
Neurosci. 5: 147–154.
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Stimulus Coding by Primary Afferent Neurons
Neuronal signaling in the auditory pathway begins with the spiral ganglion neurons that
receive transmitter released from hair cells and send their central axons to the cochlear
nucleus of the brainstem. Many decades of single fiber recordings have catalogued the
acoustic responses of these primary afferents.61 Each spiral ganglion neuron responds selectively to the frequency of sound that is optimal for the inner hair cell to which it is attached.
Each inner hair cell is the sole presynaptic partner of a group of type I afferent neurons,
numbering from 10 to 30, depending on location in the cochlea (see Figure 22.11). Both
acoustic threshold and spontaneous firing rate vary among this pool of afferents53 helping
to extend the dynamic range of the cochlea. Presumably, individual ribbon synapses of an
inner hair cell can have different release properties.62,63 The selective innervation of inner
hair cells on the mechanically tuned basilar membrane produces an array of 10,000 or so
afferent neurons that serve as frequency-labeled lines—the first stage of the tonotopically
organized auditory pathway. In addition to this pitch-is-place mechanism, phase-locked
firing of afferent action potentials to acoustic sinusoids can be used to encode frequency
up to about 3 kHz in the guinea pig64 and up to 10 kHz in the barn owl.65
Brainstem and Thalamus
Cerebral
cortex
Auditory
cortex
Medial
geniculate
nucleus
Thalamus
Inferior colliculus
Midbrain
The main auditory pathways are illustrated schematically in Figure 22.12.
Auditory fibers of the eighth nerve travel centrally and send branches
to both the dorsal and ventral cochlear nuclei.66 Second-order axons
ascend in the contralateral lateral lemniscus to innervate cells in the
inferior colliculus (the nucleus of the lateral lemniscus is a synaptic
way station for some of these fibers). Neurons in the ventral cochlear
nucleus also provide collateral branches to both the ipsilateral and
contralateral superior olivary nuclei. Third-order cells in the olivary
nuclei, in turn, send ascending fibers to the inferior colliculus. The
ascending pathway continues through the medial geniculate nucleus
of the thalamus to the auditory region on the transverse surface of the
temporal lobe of the cerebral cortex.
Each level in the auditory pathway is tonotopically mapped. However,
as one ascends higher in the auditory system, individual cells have more
complex response properties than the simple V-shaped tuning curves
of cochlear afferent neurons. For example, some cells in the inferior
colliculus67 and auditory cortex68 are only excited near threshold at
their characteristic frequency, and louder tones are inhibitory.
Sound Localization
(Dorsal)
Cochlear nuclei
(Ventral)
Medulla
Auditory
nerve
Superior olivary nuclei
Cochlea
The impressive sensitivity and frequency selectivity of the auditory
system may have evolved to improve the animal’s ability to locate a
sound in space. The advantages of doing so are obvious; long-range
signals emitted as sound waves can reveal a distant predator or prey in
FIGURE 22.12 Auditory Pathways Central auditory pathways are shown schematically on transverse sections of the medulla, midbrain, and thalamus, as well as on
a coronal section of the cerebral cortex. Auditory nerve fibers end in the dorsal and
ventral cochlear nuclei. Second-order fibers ascend to the contralateral inferior colliculus; those from the ventral cochlear nucleus also supply collaterals bilaterally to the
superior olivary nuclei. Further bilateral interaction occurs at the level of the inferior colliculus. Neurons of the inferior colliculus project to the medial geniculate nucleus of the
thalamus, which in turn projects to the auditory cortex. (After Berne and Levy, 1988.)
©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.