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Factors affecting the recording of visual-evoked potentials from the deaf cat primary auditory cortex (AI)
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Brain Research, 188 (I 980) 252-254 ff~ Elsevier/North-Holland Biomedical Press
Factors affecting the recording of visual-evoked potentials from the deaf cat primary auditory cortex (AI)
GUY REBILLARD, MIREILLE REBILLARD and RI~MY PUJOL Laboratoire de Neurophysiologie sensoriel[e, Universit~ de Provence, Centre St J~rdme, 13397 Marseille Cddex 4 (France)
(Accepted December 20th, 1979) Key words: visual responses -- evoked potentials -- deaf cat -- auditory cortex
Bonaventure and Karli 1,2 found that in mice with hereditary retinal degeneration there was a substantially enhanced auditory-evoked response in the primary visual cortex. We recently described the reverse phenomenon (Rebillard et al.6). Large visualevoked potentials (VEP) could be recorded from the primary auditory cortex (AI) of genetically deaf white cats or cats bilaterally cochleectomized during the first postnatal week. Since these results have important implication for postnatal auditory system plasticity, it seemed worthwhile to study this phenomenon further. Three aspects were studied: (l) the postnatal period during which cochleectomy is effective; (2) the delay between cochleectomy and the first appearance of VEP; and (3) the influence of electrically stimulating the auditory pathway. Four groups of cats were studied; 3 adult white cats shown to be completely deaf and 12 coloured cats in which bilateral cochleectomies were performed between one and 8 postnatal weeks. In these two groups, recordings were done in adulthood. A third group (8 coloured cats) was cochleectomized around day 15 and recordings were done between 21 days and 6 months. The last group (3 coloured cats) were also cochleectomized at 15 days of age and stimulating electrodes were chronically implanted in the inferior colliculus (IC). These cats received daily collicular stimulation consisting of trains of 1 msec square waves having an intensity of 200 #A and a frequency ranging between 1 and 10 Hz. The visual stimuli consisted of flashes presented at a rate of 1 per 2 sec. Anesthetics were ketamine (20 mg/kg i.m.) for cochleectomy and Nembutal (40 mg/kg i.p.) during cortical recordings. Visual-evoked responses were recorded using tungsten microelectrodes and transcortical macroelectrodes. From the group of cats whose cochleas were destroyed between 1 and 8 weeks post-partum, only those deafferented during the first 3 postnatal weeks (8 cats) showed visual responses in adulthood. The shape and latency of such potentials (Fig. 1) agree well with those previously reported 6.
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2
;" 4
loOpv I 20ms Fig. 1. Examples of visual responses recorded in the primary auditory cortex of an adult cat cochleectomized early in development. In the remaining 4 cats, which where cochleectomized between 4 and 8 weeks of age, it was impossible to record such potentials. Only one of the 3 genetically deaf white cats showed visual responses in AI. All animals in the group cochleectomized at day 15 showed visual responses in AI, regardless of the age at recording. The 3 kittens deafferented at day 15 which then received daily electrical stimulation of the IC did not show any visual responses in AI, one month after cochleectomies. At this time, the electrical IC stimuli still evoked potentials in both AI areas. The above data confirm our previous findings 6 that complete cochlear destruction results in the appearance of visual-evoked potentials in AI. However, in order to obtain this phenomenon, cochleectomy must be performed before the end of the third postnatal week. This fact suggests the existence of a critical period and could explain why 2 of the 3 genetically deaf white cats tested did not show visual responses in AI. As described in a previous study 7, and in contrast with the findings of Bosher and Hallpike 3 and Mair 4, in the white cat there are large individual differences in the timing of cochlear degeneration. In these animals, deafness can appear anywhere between 7 days and 4 months post-partum. It is possible that in adult deaf white cats visual potentials in AI are observed only when deafness appears before the critical period (first 3 weeks). The anatomical basis for the above phenomenon remains to be determined. Two hypotheses may be suggested. The basis of the VEP in AI of cochleectomized kittens may be in new pathways formed after deafferentation. Alternately cochleectomy may simply stabilize existing visual pathways to AI. In support of the latter it is known that
254 early in kitten postnatal development sensory cortical areas are not well defined, since A I receives both auditory and visual inputs 5. Besides, as shown above, VEP could be recorded as soon as the animal had recovered from peripheral surgery. Therefore, it seems likely that the appearance of visual-evoked potential in the AI of cats cochleectomized at 15 days of age was due to the reinforcement of existing visual pathways to the primary auditory cortex. Lack of excitation in the auditory pathway seems to be critical for the continued appearance o f VEP in AI, since it is absent in incomplete deaf cats 8 and, as demonstrated here, in cochleectomized kittens electrically stimulated in IC. In general, it would appear that early visual connection to the auditory primary area, probably genetically programmed, may continue to function in adulthood if AI is deprived o f auditory inputs before the end of the first postnatal month. The functional significance o f ' a b n o r m a l ' visual responses in AI remains for further study. This research was supported by grants from I N S E R M (CRL), D G R S T (BRDD N ) and C N R S ( R C P 537). The authors are indebted to Dr. A. Shnerson for assistance in writing this manuscript.
1 Bonaventure, N. et Karli, P., Apparition au niveau du cortex visuel de potentiels 6voqu6s d'origine auditive chez la souris priv6e de photor6cepteurs, J. PhysioL (Paris), 70 (1968) 407. 2 Bonaventure, N. et Karli, P., Nouvelles donn6es sur les potentiels d'origine auditive evoqu6s au niveau du cortex visuel chez la souris, C.R. Soc. Biol. (Paris), 163 (1969) 1705-1708. 3 Bosher, S. K. and Hallpike, C. S., Observation on the histological features, development and pathogenesis of the inner ear degeneration of the deaf white cat, Proc. roy. Soc. B, 162 (1965) 147-170. 4 Mair, I. W. S., Hereditary deafness in the white cat. IlL Cochlear histopathology, Acta otolaryng. (Stockh.), suppl. 314 (1973) 23-35. 5 Marry, R., D6veloppement postnatal des r6ponses sensorielles du cortex c6r6bral chez le chat et le lapin, Arch. Anat. micr. Morph. exp., 51 (1962) 129-264. 6 Rebillard, G., Carlier, E., Rebillard, M. and Pujol, R., Enhancement of visual responses on the primary auditory cortex of the cat after an early destruction of cochlear receptors, Brain Research, 129 (1977) 162-164. 7 R.ebillard, G., Rebillard, M., Carlier, E. and Pujol, R., Histophysiological relationships in the deaf white cat auditory system, Acta otolaryng. (Stockh.), 82 (1976) 48-56.
Brain Research, 188 (I 980) 252-254 ff~ Elsevier/North-Holland Biomedical Press
Factors affecting the recording of visual-evoked potentials from the deaf cat primary auditory cortex (AI)
GUY REBILLARD, MIREILLE REBILLARD and RI~MY PUJOL Laboratoire de Neurophysiologie sensoriel[e, Universit~ de Provence, Centre St J~rdme, 13397 Marseille Cddex 4 (France)
(Accepted December 20th, 1979) Key words: visual responses -- evoked potentials -- deaf cat -- auditory cortex
Bonaventure and Karli 1,2 found that in mice with hereditary retinal degeneration there was a substantially enhanced auditory-evoked response in the primary visual cortex. We recently described the reverse phenomenon (Rebillard et al.6). Large visualevoked potentials (VEP) could be recorded from the primary auditory cortex (AI) of genetically deaf white cats or cats bilaterally cochleectomized during the first postnatal week. Since these results have important implication for postnatal auditory system plasticity, it seemed worthwhile to study this phenomenon further. Three aspects were studied: (l) the postnatal period during which cochleectomy is effective; (2) the delay between cochleectomy and the first appearance of VEP; and (3) the influence of electrically stimulating the auditory pathway. Four groups of cats were studied; 3 adult white cats shown to be completely deaf and 12 coloured cats in which bilateral cochleectomies were performed between one and 8 postnatal weeks. In these two groups, recordings were done in adulthood. A third group (8 coloured cats) was cochleectomized around day 15 and recordings were done between 21 days and 6 months. The last group (3 coloured cats) were also cochleectomized at 15 days of age and stimulating electrodes were chronically implanted in the inferior colliculus (IC). These cats received daily collicular stimulation consisting of trains of 1 msec square waves having an intensity of 200 #A and a frequency ranging between 1 and 10 Hz. The visual stimuli consisted of flashes presented at a rate of 1 per 2 sec. Anesthetics were ketamine (20 mg/kg i.m.) for cochleectomy and Nembutal (40 mg/kg i.p.) during cortical recordings. Visual-evoked responses were recorded using tungsten microelectrodes and transcortical macroelectrodes. From the group of cats whose cochleas were destroyed between 1 and 8 weeks post-partum, only those deafferented during the first 3 postnatal weeks (8 cats) showed visual responses in adulthood. The shape and latency of such potentials (Fig. 1) agree well with those previously reported 6.
253
2
;" 4
loOpv I 20ms Fig. 1. Examples of visual responses recorded in the primary auditory cortex of an adult cat cochleectomized early in development. In the remaining 4 cats, which where cochleectomized between 4 and 8 weeks of age, it was impossible to record such potentials. Only one of the 3 genetically deaf white cats showed visual responses in AI. All animals in the group cochleectomized at day 15 showed visual responses in AI, regardless of the age at recording. The 3 kittens deafferented at day 15 which then received daily electrical stimulation of the IC did not show any visual responses in AI, one month after cochleectomies. At this time, the electrical IC stimuli still evoked potentials in both AI areas. The above data confirm our previous findings 6 that complete cochlear destruction results in the appearance of visual-evoked potentials in AI. However, in order to obtain this phenomenon, cochleectomy must be performed before the end of the third postnatal week. This fact suggests the existence of a critical period and could explain why 2 of the 3 genetically deaf white cats tested did not show visual responses in AI. As described in a previous study 7, and in contrast with the findings of Bosher and Hallpike 3 and Mair 4, in the white cat there are large individual differences in the timing of cochlear degeneration. In these animals, deafness can appear anywhere between 7 days and 4 months post-partum. It is possible that in adult deaf white cats visual potentials in AI are observed only when deafness appears before the critical period (first 3 weeks). The anatomical basis for the above phenomenon remains to be determined. Two hypotheses may be suggested. The basis of the VEP in AI of cochleectomized kittens may be in new pathways formed after deafferentation. Alternately cochleectomy may simply stabilize existing visual pathways to AI. In support of the latter it is known that
254 early in kitten postnatal development sensory cortical areas are not well defined, since A I receives both auditory and visual inputs 5. Besides, as shown above, VEP could be recorded as soon as the animal had recovered from peripheral surgery. Therefore, it seems likely that the appearance of visual-evoked potential in the AI of cats cochleectomized at 15 days of age was due to the reinforcement of existing visual pathways to the primary auditory cortex. Lack of excitation in the auditory pathway seems to be critical for the continued appearance o f VEP in AI, since it is absent in incomplete deaf cats 8 and, as demonstrated here, in cochleectomized kittens electrically stimulated in IC. In general, it would appear that early visual connection to the auditory primary area, probably genetically programmed, may continue to function in adulthood if AI is deprived o f auditory inputs before the end of the first postnatal month. The functional significance o f ' a b n o r m a l ' visual responses in AI remains for further study. This research was supported by grants from I N S E R M (CRL), D G R S T (BRDD N ) and C N R S ( R C P 537). The authors are indebted to Dr. A. Shnerson for assistance in writing this manuscript.
1 Bonaventure, N. et Karli, P., Apparition au niveau du cortex visuel de potentiels 6voqu6s d'origine auditive chez la souris priv6e de photor6cepteurs, J. PhysioL (Paris), 70 (1968) 407. 2 Bonaventure, N. et Karli, P., Nouvelles donn6es sur les potentiels d'origine auditive evoqu6s au niveau du cortex visuel chez la souris, C.R. Soc. Biol. (Paris), 163 (1969) 1705-1708. 3 Bosher, S. K. and Hallpike, C. S., Observation on the histological features, development and pathogenesis of the inner ear degeneration of the deaf white cat, Proc. roy. Soc. B, 162 (1965) 147-170. 4 Mair, I. W. S., Hereditary deafness in the white cat. IlL Cochlear histopathology, Acta otolaryng. (Stockh.), suppl. 314 (1973) 23-35. 5 Marry, R., D6veloppement postnatal des r6ponses sensorielles du cortex c6r6bral chez le chat et le lapin, Arch. Anat. micr. Morph. exp., 51 (1962) 129-264. 6 Rebillard, G., Carlier, E., Rebillard, M. and Pujol, R., Enhancement of visual responses on the primary auditory cortex of the cat after an early destruction of cochlear receptors, Brain Research, 129 (1977) 162-164. 7 R.ebillard, G., Rebillard, M., Carlier, E. and Pujol, R., Histophysiological relationships in the deaf white cat auditory system, Acta otolaryng. (Stockh.), 82 (1976) 48-56.