The study investigates early postnatal development of local field potentials (LFPs) in the primary auditory cortex of hearing and congenitally deaf cats. In hearing cats, LFPs elicited by electrical intracochlear stimulation demonstrated developmental changes in mid-latency range, including reductions in peak and onset latencies of individual waves and a maturation of their shape and latencies during the first 2 months of life. In long latency range (>80 ms), the P(1)/N(1) response appeared after the fourth week of life and further increased in amplitude and decreased in latency, reaching mature shapes between the fourth and sixth months after birth (p.n.). Cortical activated areas became increasingly smaller during the first 3 months of life, reaching mature values at the fourth month p.n. The layer-specific pattern of synaptic activity matured 4 months p.n. In congenitally deaf cats, the developmental pattern was different. The lowest cortical LFP thresholds were significantly smaller than in hearing controls, demonstrating a "hypersensitivity" to sensory inputs. The development of N(b) waves was delayed and altered and the long latency responses became smaller than in controls at the second and third months. The activated areas remained smaller than in controls until the third month, then they increased rapidly and exceeded the activated areas of age-matched controls. From the fourth month on, the activated areas decreased again and smaller synaptic currents were found in deaf cats than in controls. The presented data demonstrate that functional development of the auditory cortex critically depends on auditory experience.
Unilateral deafness has a high incidence in children. In addition to children who are born without hearing in one ear, children with bilateral deafness are frequently equipped only with one cochlear implant, leaving the other ear deaf. The present study investigates the effects of such single-sided deafness during development in the congenitally deaf cat. The investigated animals were either born with unilateral deafness or received a cochlear implant in one ear and were subjected to chronic monaural stimulation. In chronically stimulated animals, implantation ages were at the following three critical developmental points: 'early' during the peak of functional cortical synaptogenesis in deaf animals; 'intermediate' at the age when synaptic activity in the deaf cats dropped to the level of hearing control cats and finally, 'late' at the age when the evoked synaptic activity fell below the level of hearing control cats. After periods of unilateral hearing, local field potentials were recorded from the cortical surface using a microelectrode at ∼100 recording positions. Stimulation was with cochlear implants at both ears. The measures evaluated were dependent only on the symmetry of aural input: paired differences of onset latencies and paired relations of peak amplitudes of local field potentials. A massive reorganization of aural preference in favour of the hearing ear was found in these measures if the onset of unilateral hearing was early (before or around the peak of functional synaptogenesis). The effect was reduced if onset of unilateral hearing was in the intermediate period, and it disappeared if the onset was late. In early onset of unilateral deafness, the used ear became functionally dominant with respect to local field potential onset latency and amplitude. This explains the inferior outcome of implantations at the second-implanted ear compared with first-implanted ear in children. However, despite a central disadvantage for the deaf ear, it still remained capable of activating the auditory cortex. Appropriate training may thus help to improve the performance at the second-implanted ear. In conclusion, periods of monaural stimulation should be kept as short as possible, and training focused on the deaf ear should be introduced after delayed second implantation in children.
In congenitally deaf cats, the central auditory system is deprived of acoustic input because of degeneration of the organ of Corti before the onset of hearing. Primary auditory afferents survive and can be stimulated electrically. By means of an intracochlear implant and an accompanying sound processor, congenitally deaf kittens were exposed to sounds and conditioned to respond to tones. After months of exposure to meaningful stimuli, the cortical activity in chronically implanted cats produced field potentials of higher amplitudes, expanded in area, developed long latency responses indicative of intracortical information processing, and showed more synaptic efficacy than in naïve, unstimulated deaf cats. The activity established by auditory experience resembles activity in hearing animals.
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 electro-stimulated over a period of 2.0-5.5 months using a monopolar single-channel compressed analogue stimulation strategy (VIENNA-type 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 microV 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.
The present study investigates the functional deficits of naive auditory cortices in adult congenitally deaf cats. For this purpose, their auditory system was stimulated electrically using cochlear implants. Synaptic currents in cortical layers were revealed using current source density analyses. They were compared with synaptic currents found in electrically stimulated hearing cats. The naive auditory cortex showed significant deficits in synaptic activity in infragranular cortical layers. Furthermore, there was also a deficit of synaptic activities at longer latencies (>30 ms). The 'cortical column' was not activated in the well-defined sequence found in normal hearing cats. These results demonstrate functional deficits as a consequence of congenital auditory deprivation. Similar deficits are likely in congenitally deaf children.
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