Synaptic plasticity after chemical deafening and electrical stimulation of the auditory nerve in cats (original) (raw)
Related papers
The Journal of Comparative Neurology, 1998
It is well known that experimentally induced cochlear damage produces structural, physiological, and biochemical alterations in neurons of the cochlear nucleus. In contrast, much less is known with respect to the naturally occurring cochlear pathology presented by congenital deafness. The present study attempts to relate organ of Corti structure and auditory nerve activity to the morphology of primary synaptic endings in the cochlear nucleus of congenitally deaf white cats. Our observations reveal that the amount of sound-evoked spike activity in auditory nerve fibers influences terminal morphology and synaptic structure in the anteroventral cochlear nucleus. Some white cats had no hearing. They exhibited severely reduced spontaneous activity and no sound-evoked activity in auditory nerve fibers. They had no recognizable organ of Corti, presented Ͼ90% loss of spiral ganglion cells, and displayed marked structural abnormalities of endbulbs of Held and their synapses. Other white cats had partial hearing and possessed auditory nerve fibers with a wide range of spontaneous activity but elevated sound-evoked thresholds (60-70 dB SPL). They also exhibited obvious abnormalities in the tectorial membrane, supporting cells, and Reissner's membrane throughout the cochlear duct and had complete inner and outer hair cell loss in the base. The spatial distribution of spiral ganglion cell loss correlated with the pattern of hair cell loss. Primary neurons of hearing-impaired cats displayed structural abnormalities of their endbulbs and synapses in the cochlear nucleus which were intermediate in form compared to normal and totally deaf cats. Changes in endbulb structure appear to correspond to relative levels of deafness. These data suggest that endbulb structure is significantly influenced by sound-evoked auditory nerve activity.
The effects of congenital deafness on auditory nerve synapses and globular bushy cells in cats
Hearing Research, 2000
It is well known that auditory deprivation affects the structure and function of the central nervous system. Congenital deafness represents one form of deprivation, and in the adult white cat, it has been shown to have a clear effect upon the synaptic interface between endbulbs of Held and spherical bushy cells. It is not known, however, whether all primary synapses are affected and/or whether they are affected in the same way and to the same extent. Thus, we studied a second neuronal circuit in the deaf white cat involving modified (small) endbulbs and globular bushy cells. Compared to normal hearing cats, modified endbulbs of congenitally deaf cats were 52.2% smaller but unchanged in structural complexity. There was also a striking loss of extracellular space between ending and cell body. The somata of postsynaptic globular bushy cells were 13.4% smaller and had enlarged postsynaptic densities. These data reveal that axosomatic synapses demonstrate abnormal structure as a consequence of deafness and that the extent of the abnormalities can vary with respect to the circuits involved. The implication of these observations is that synaptic anomalies would introduce differential delays within separate circuits, thereby desynchronizing neural activity from sound stimuli. This loss of synchronization could in turn disrupt temporal processing and compromise a host of related functions, including language comprehension.
Hearing after Congenital Deafness: Central Auditory Plasticity and Sensory Deprivation
Cerebral Cortex, 2002
The congenitally deaf cat suffers from a degeneration of the inner ear. The organ of Corti bears no hair cells, yet the auditory afferents are preserved. Since these animals have no auditory experience, they were used as a model for congenital deafness. Kittens were equipped with a cochlear implant at different ages and electrostimulated over a period of 2.0-5.5 months using a monopolar single-channel compressed analogue stimulation strategy (VIENNAtype signal processor). Following a period of auditory experience, we investigated cortical field potentials in response to electrical biphasic pulses applied by means of the cochlear implant. In comparison to naive unstimulated deaf cats and normal hearing cats, the chronically stimulated animals showed larger cortical regions producing middle-latency responses at or above 300 µV amplitude at the contralateral as well as the ipsilateral auditory cortex. The cortex ipsilateral to the chronically stimulated ear did not show any signs of reduced responsiveness when stimulating the 'untrained' ear through a second cochlear implant inserted in the final experiment. With comparable duration of auditory training, the activated cortical area was substantially smaller if implantation had been performed at an older age of 5-6 months. The data emphasize that young sensory systems in cats have a higher capacity for plasticity than older ones and that there is a sensitive period for the cat's auditory system.
Sound Following Conductive Hearing Loss
2005
Conductive hearing loss (CHL) is an attenuation of signals stimulating the cochlea, without damage to the auditory end organ. It can cause central auditory processing deficits that outlast the CHL itself. Measures of oxidative metabolism show a decrease in activity of nuclei receiving input originating at the affected ear, but surprisingly, an increase in the activity of second order neurons of the opposite ear. In normal hearing animals, contralateral sound produces an inhibitory response to broadband noise in approximately one third of ventral cochlear nucleus (VCN) neurons. Excitatory responses also occur but are very rare. We looked for changes in the binaural properties of neurons in the VCN of guinea pigs at intervals immediately, 1 day, 1 week and 2 weeks following the induction of a unilateral CHL by ossicular disruption. CHL was always induced in the ear ipsilateral to the VCN from which recordings were made. The main observations were: i. Ipsilateral excitatory thresholds were raised by at least 40dB. ii. Contralateral inhibitory responses showed a small but statistically significant immediate decrease followed by an increase, returning to normal by 14 days. iii. There was a large increase in the proportion of units with excitatory responses to contralateral BBN. The increase was immediate and lasting. The latencies of the excitatory responses were at least 6 ms, consistent with activation by a path involving several synapses and inconsistent with crosstalk. The latencies and rate-level functions of contralateral excitation were similar to those seen occasionally in normal hearing animals, suggesting an up-regulation of an existing pathway. In conclusion, contralateral excitatory inputs to the VCN exist, which are not normally effective, and can compensate rapidly for large changes in afferent input. 3 Alibardi L. Cytology, synaptology and immunocytochemistry of commissural neurons and their putative axonal terminals in the dorsal cochlear nucleus of the rat. Anat Anz 182: 207-220, 2000. Alibardi L. Putative inhibitory collicular boutons contact large neurons and their dendrites in the dorsal cochlear nucleus of the rat. J Submicrosc Cytol Pathol 34: 433-446, 2002. Alibardi L. Ultrastructural and immunocytochemical characterization of commissural neurons in the ventral cochlear nucleus of the rat. Anat Anz 180: 427-438, 1998. Babalian AL, Jacomme AV, Doucet JR, Ryugo DK, and Rouiller EM. Commissural glycinergic inhibition of bushy and stellate cells in the anteroventral cochlear nucleus. Neuroreport 13: 555-558, 2002. Benson T and Brown M. Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses. J Comp Neurol 365: 27-41, 1996. Benson TE and Brown MC. Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus. J Comp Neurol 295: 52-70, 1990. Brown M and TE. B. Transneuronal labeling of cochlear nucleus neurons by HRPlabeled auditory nerve fibers and olivocochlear branches in mice. J Comp Neurol 321: 645-665., 1992. Brown MC, Liberman MC, Benson TE, and Ryugo DK. Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278: 591-603, 1988. Brown MC, Pierce S, and Berglund AM. Cochlear-nucleus branches of thick (medial) olivocochlear fibers in the mouse: a cochleotopic projection. J Comp Neurol 303: 300-315, 1991. Calford MB. Dynamic representational plasticity in sensory cortex. Neuroscience 111: 709-738, 2002. Cant NB and Casseday JH. Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei.PG -457-76. J Comp Neurol 247, 1986. Cant NB and Gaston KC. Pathways connecting the right and left cochlear nuclei. . Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices. Hear Res 164: 59-68, 2002. Clerici WJ and Coleman JR. 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Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus. Hearing Research 140: 165-172, 2000. Kaltenbach JA, Godfrey DA, Neumann JB, McCaslin DL, Afman CE, and Zhang JS. Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift. Hearing Research 124: 78-84, 1998. Kaltenbach JA and McCaslin DL. Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: A possible neural correlate of tinnitus. Auditory Neuroscience 3: 57-78, 1996. Kaltenbach JA, Zhang JS, and Afman CE. Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hearing Research 147: 282-292, 2000. 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Brain Research, 2015
Perceptual performance in persons with hearing loss, especially those using devices to restore hearing, is not fully predicted by traditional audiometric measurements designed to evaluate the status of peripheral function. The integrity of auditory brainstem synapses may vary with different forms of hearing loss, and differential effects on the auditory nerve-brain interface may have particularly profound consequences for the transfer of sound from ear to brain. Loss of auditory nerve synapses in ventral cochlear nucleus (VCN) has been reported after acoustic trauma, ablation of the organ of Corti, and administration of ototoxic compounds. The effects of gradually acquired forms deafness on these synapses are less well understood. We investigated VCN gross morphology and auditory nerve synapse integrity in DBA/2J mice with early-onset progressive sensorineural hearing loss. Hearing status was confirmed using auditory brainstem response audiometry and acoustic startle responses. We found no change in VCN volume, number of macroneurons, or number of VGLUT1-positive auditory nerve terminals between young adult and older, deaf DBA/2J. Cell-type specific analysis revealed no difference in the number of VGLUT1 puncta contacting bushy and multipolar cell body profiles, but the terminals were smaller in deaf DBA/2J mice. Transmission electron microscopy confirmed the presence of numerous healthy, vesicle-filled auditory nerve synapses in older, deaf DBA/2J mice. The present results suggest that synapses can be preserved over a relatively long time-course in gradually acquired deafness. Elucidating the mechanisms supporting survival of central auditory nerve synapses in models of acquired deafness may reveal new opportunities for therapeutic intervention.
Ultrastructural Changes in Primary Endings of Deaf White Cats
Otolaryngology-Head and Neck Surgery, 1997
Changes in brain structure occur as a consequence of altered experience. During maturation of the auditory nervous system, sensory deprivation is known to cause cell loss, abnormal axonal projections, and synaptic alterations. These animal data may be relevant to clinical observations that cochlear implants provide superior benefit for individuals who become deaf postlingually compared with those who become deaf prelingually. That is, implantation appears most efficacious if it occurs after functional connections are established but before deprivation-induced changes in the central auditory system. After this period, synaptic reorganization may underlie the diminished effectiveness of cochlear implants.
Morphological changes in the cochlear nucleus of congenitally deaf white cats
Brain Research, 1996
Investigations in animal models and humans have indicated that congenital deafness produces degenerative changes in the central auditory pathway. The cochlear nucleus is the first central structure that receives cochlear input, and may be considered the origin of ascending auditory pathways. In this context, we studied congenitally deaf white cats, who express early onset cochlear receptor loss, in order to assess the nature of structural changes in cells of the cochlear nucleus. It is conceivable that pathologic alterations in higher auditory structures are transneuronally distributed through this nucleus. The cochlear nuclei of nonwhite cats with normal hearing were compared to those of deaf white cats exhibiting hearing loss in excess of 70 dB SPL. The cochlear nuclei of the deaf white cats were smaller in volume by roughly 50%, with the ventral and dorsal divisions being equally affected. Cell body silhouette area was determined for spherical bushy cells of the anteroventral cochlear nucleus (AVCN), pyramidal cells of the dorsal cochlear nucleus (DCN), sensory neurons from the principal trigeminal nucleus, and motoneurons of the facial nucleus. We found no statistical difference in neuronal cell body size between nonauditory neurons of these two groups of cats, whereas auditory neurons of deaf white cats were 30.8-39.4% smaller than those of normal cats. These data imply that neuronal changes in congenitally deaf cats are specific to the auditory pathway. Although cochlear nucleus volume loss was uniform for both divisions, there was a differential effect on cell density: AVCN cell density increased by 40%, whereas DCN cell density was relatively unaffected (10% increase). Astrocyte density was also greater in the AVCN (52%) compared to that in the DCN (5%). These observations reveal a differential impact on cells in the cochlear nucleus to congenital deafness, suggesting selective processing impairment at this level. If similar patterns of degeneration occur in humans, such pathologies may underlie reduced processing of input from cochlear implants in congenitally deaf adults. changes in physiological response properties. Congenitally deaf animals, however, offer a naturally occurring model of deafness and may offer an alternative approach to studies of auditory system plasticity associated with cochlear dysfunction .
Auditory neuroplasticity, hearing loss and cochlear implants
Cell and Tissue Research, 2014
Data from our laboratory show that the auditory brain is highly malleable by experience. We establish a base of knowledge that describes the normal structure and workings at the initial stages of the central auditory system. This research is expanded to include the associated pathology in the auditory brain stem created by hearing loss. Utilizing the congenitally deaf white cat, we demonstrate the way that cells, synapses, and circuits are pathologically affected by sound deprivation. We further show that the restoration of auditory nerve activity via electrical stimulation through cochlear implants serves to correct key features of brain pathology caused by hearing loss. The data suggest that rigorous training with cochlear implants and/or hearing aids offers the promise of heretofore unattained benefits.