252
Neuroscience Letters, 111 (1990) 252 257 Elsevier ScientificPublishers Ireland Ltd.
NSL 06769
Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat W.R. Webster l, C. Batini l, C. Buisseret-Delmas l, C.
C o m p o i n t l,
M. G u e g a n I a n d M. T h o m a s s e t 2 ILahoratoire de Physiologie de la Motrkit~;, CNRS URA 385, Universit~ Pierre et Marie Curie, Paris (France) and~'INSERM, U 120, Le Vesinet (France)
(Received 27 July 1989: Revised version received 29 November 1989: Accepted 1 December 1989) Key word~: Calbindin: 7-Aminobutyricacid: Nucleus trapezoid body: Colocalization Using immunocytochemical methods, both calbindin and GABA were found to be colocalized in the somas of all the cells of the medial nucleus of the trapezoid body (NMTB) of the rat auditory system. In the lateral superior olive (LSO), calbindin was also found in the terminals but not in the cells. Some terminal labelling was found in the medial superior olive (MSO). GABA was also found in the somas of some cells in both LSO and MSO, but most of the labelling was in terminals. In the rat, calbindin appears to be more involved in a pathway that detects interaural intensity differences.
Ca 2 + ions play a key role in the operation of a variety of central nervous system mechanisms, including the release of t r a n s m i t t e r a n d h o r m o n e s [7] a n d light adaptation in rods and cones [8]. They may also be involved in m e m o r y [4]. Inflowing Ca 2+ ions appear to bind to intracellular C a - b i n d i n g proteins such as calbindin, a 28 k D a vitamin D-induced c a l c i u m - b i n d i n g protein [6]. Konishi and his coworkers [15] have argued that the d i s t r i b u t i o n of such e n d o g e n o u s c a l c i u m - b i n d i n g proteins can provide much i n f o r m a t i o n a b o u t the o r g a n i z a t i o n of the brain, but their explicit functional role remains unclear. Konishi and his colleagues [(5] have proposed a challenging functional correlation between the d i s t r i b u t i o n of c a l b i n d i n a n d phaselocking of cells in the a u d i t o r y system of the b a r n owl ( T y t o alba). They used i m m u nocytochemical techniques to show that calbindin is m a i n l y localized to an a u d i t o r y pathway which is involved in phase-locking for the detection of differences in the timing of sounds arriving at the two ears [13, 14]. A n interaural intensity detecting pathway was not labelled with calbindin [15]. T a k a h a s h i et al. [15] do point out that there has been no detailed study of the distri-
Corre,7)ondence: W.R. Webster, Laboratoire de Physiologiede la Motricit6, CNRS URA 385, Universit6 Pierre et Marie Curie, Paris, France.
0304-3940/90/S 03.50 ~ 1990ElsevierScientificPublishers Ireland Ltd.
253 bution of calbindin in the central mammalian auditory system, which could provide a test of the generality of their claim that calbindin is involved in mechanisms that underlie the preservation of the timing of incoming signals in the postsynaptic somata. The present study examined the distribution of calbindin in the rat auditory system and its correlation with that of GABA, which colocalizes with calbindin in the cerebellum [2]. GABA has also been found colocalized with another calciumbinding protein, parvalbumin (PV), in the rat cerebral cortex and cerebellum [5]. Fourteen rats were perfused intracardiacally with a solution of 4% paraformaldehyde in phosphate buffer (0.1 M; pH 7.4) and their brains removed. Free-floating, 40-/~m-thick vibratome sections were cut. Sections from 7 animals were incubated overnight with anti-calbindin 28 kDa serum (1:4000 in PBS) raised in rabbits immunized with purified rat kidney calbindin [6]. Antiserum specificity was checked by Ouchterlony double-immunodiffusion, radioimmunoassay [16] and immunoprecipitation [6]. The second incubation was carried out with goat anti-rabbit diluted to 1:200 in PBS for 1 h 30 min. The final incubation was in rabbit PAP (1:400). The calbindin reactive sites were visualized using 0.5% diaminobenzidine (DAB) by incubating with 0.5% DAB, 0.1% H202 in 0.1 M Tris-HCl, pH 7.6 for 15 rain. The other 7 animals were treated for GABA immunocytochemistry using methods already described in detail [3]. Sections from
Fig. I. A: photomicrographof the rat superior olivarycomplex showingimmunohistochemicallabelling for calbindin. B: enlargement of N M T B at the position of the arrow. C: enlargementof LSO at the position of the arrow.
254
2 GABA and 2 calbindin animals were counterstained for Nisst. Two further animals were perfused and their brains sectioned at 10/~m after paraffin embedding. The sections for one animal was treated for calbindin and those of the other for GABA. Staining for both calbindin and GABA occurred throughout the auditory pathway (the interstitial nucleus of the auditory nerve, the cochlear nuclei, the superior olivary complex, the nuclei of the lateral lemniscus, the inferior colliculus, the medial geniculate body and the auditory cortex). The details of this labelling will be reported later; the present report concentrates on the labelling in the superior olivary complex, as this is the region in the mammalian brain which contains the beginning of both the timing and intensity pathways. In contrast to the finding that calbindin was restricted to a time difference-detecting pathway, we found most calbindin (Fig. I A, B) in the medial nucleus of the trapezoid body (NMTB), which is involved in a pathway for detecting interaural intensity differences [t]. The somata of the cells were labelled in NMTB (Fig. 1A, B). The NMTB has an inhibitory projection to cells of the lateral superior olive (LSO) which are sensitive to interaural intensity differences of high frequency sounds [1]. There is also considerable labelling in the LSO but it is largely confined to terminals surrounding unstained somata (Fig. IA, C). The medial super-
2,
Fig. 2. A: photomicrograph of the rat superior olivary complex showing immunohistochemical labelling for GABA. B: enlargement of labelling at position of solid arrow in NMTB. C: enlargement of labelling at position of open arrow in LSO.
255
ior olive (MSO) is the first site for detecting interaural timing differences of low frequency sounds in the mammalian brain but unlike N M T B no somata were labelled. Like LSO, MSO has only terminals labelled but to a lesser extent (Fig. IA). It is only in N M T B that the somata of cells are clearly labelled for calbindin in the superior olive. The pattern of GABA immunoreactivity in the superior olive was similar in some respects to the calbindin pattern. All the cell somata were GABA-positive in N M T B (Fig. 2A, B). The proportion of GABA and calbindin labelling was checked by counting the number of stained cells in the N M T B before and after counterstaining for Nissl. The same number of cells were observed before and after counterstaining and no cells were found which were stained for Nissl but not for the antibody, therefore it can be concluded that calbindin and GABA are colocalized in the cells of NMTB. The labelling patterns for calbindin and GABA in other parts of the superior olivary complex were different. In the LSO, the somata of several cells were GABA-positive and the labelling also involved terminals around stained and unstained somata (Fig. 2A, C). GABA labelling in the MSO was similar to that of the LSO (Fig. 2A). For all of the superior olive, the same pattern of labelling was seen with 10/tm sections as that found in all the animals with 40/zm sections. This is illustrated in Fig. 3A, in which cells in N M T B are labelled with calbindin and in Fig. 3B where they are labelled with GABA, thus confirming similar results obtained with 40/zm sections. The results of these experiments indicate that the distribution of calbindin in the auditory system of the rat is different from that of the barn owl [15]. Calbindin is not restricted to a pathway involved in the detection of interaural time differences. It appears to be more closely involved in a pathway that detects interaural intensity differences, and which is not labelled for calbindin in the barn owl [15]. While the rat system appears to be different to that of the barn owl, it is not possible to conclude that calbindin is not involved in the time pathway as there is some terminal
Fig. 3. A: photomicrograph of a 10/lm section showing immunocytochemical labelling for calbindin m NMTB. B: a photomicrograph of a 10/Jm section showing immunocytochemical labelling for GABA.
256
labelling in MSO, but it is clear that calbindin is more heavily localized in the intensity pathway. Takahashi et al. [15] have also suggested that calbindin might be associated with the tonic release of neurotransmitter. Sans et al. [12] have shown that calbindin is localized in the vestibular Type II hair cells which have a high tonic rate of firing. Type I hair cells, which fire irregularly, are only weakly immunoreactive. If this were the sole function for calbindin, most of the cells in MSO and LSO should be heavily labelled because when they are excited they tend to fire in a sustained tonic manner [1]. Perhaps the most significant finding in the present study is that calbindin is colocalized with GABA in the cells of NMTB, just as calbindin and GABA are colocalized in the Purkinje cells of the cerebellum [2]. Calbindin, in both instances, may be involved in the release of this inhibitory transmitter. Celio [5] has also shown that GABA and PV are colocalized in the rat cerebellum, and suggests that calcium-binding proteins support the 3 characteristics of GABA neurons: high firing rate, high metabolic activity and receiving mainly excitatory afferents which dominate the dendritic and somatic surface thus allowing GABA neurons to be electrically and metabolically more active than their companion neurons [5]. However, many neurons in the auditory system fire at high rates but they contain neither GABA nor calbindin (for example most of the cells in LSO and MSO in the present study). The high concentration of this calcium-binding protein in the GABA cells of N M T B may be due to the presence and activity of the inhibitory transmitter GABA itself. However, the work of Moore and Caspary [9] on binaural inhibition in the LSO of the chinchilla does not entirely support this suggestion. They tbund that both GABA and glycine could mimic binaural inhibition in LSO, but that only a glycine antagonist and not a GABA antagonist blocked this effect. They concluded that inhibition in LSO arising from cells in NMTB was glycinergic rather than GABAergic. However, as all the cells in rat N M T B contained GABA, the cells projecting to LSO must also contain GABA. The principal cell of N M T B is innervated by a very large synapse (Calyce of Held) and it is these cells which provide the inhibitory projection to LSO. It should be pointed out that the published evidence for this projection comes from work on the cat [1], but unpublished HRP studies of rat N M T B from this laboratory confirm this general projection. Another possibility is that the principal cells of NMTB contain glycine as well as GABA and calbindin. In the cat, cells in NMTB are strongly immunoreactive for glycine [11, 18] but neither study reported labelling for GABA. Further studies on the role of glycine in the rat N M T B are required to clarify the relationship between GABA, glycine and calbindin. 1 Aitkin, L.M., trvine, D.R.F. and Webster W.R.. Central neural mechanisms of hearing. In I. DarianSmith (Ed.), Handbook of Physiology, Section 1: The Nervous System, Vol. 3, Sensory Processes, ch. 16, American Physiological Society, Bethesda, 1984, pp. 675 737. 2 Batini, C., Cerebellar localization and cotocalization of GABA and calcium binding protein vitamin [)-dependent 28 Kd, Arch. ltal. Biol., in press. 3 Batini, C., Buisseret-Delmas, C., Compoint, C. and Daniel, H., The GABAergic neurones of the cerebellar nuclei in the rat: projections to the cerebellar cortex, Neurosci. Lett., 99 (1989) 251 256.
257 4 Brown, T.H., Chapman, P.F., Kairiss, E.W. and Keenan, C.L., Long-term synaptic potentiation, Science, 242 (1988) 724-728. 5 Celio, M.R., Parvalbumin in most y-aminobutyric acid-containing neurons of the rat cerebral cortex, Science, 231 (1986) 995-997. 6 Intrator, S., Elion, J., Thomasset, M. and Brehier, A., Purification, immunological and biochemical characterization of rat 28-K Da cholecalcin (cholecalciferol-induced CaBP's): identity between renal and cerebellar cholecalcins, Biochem. J., 231 (I 985) 89-95. 7 Kretsinger, R.H., Calcium in neurobiology: a general theory of function and evolution. In F.O. Schmitt and F.G. Worden (Eds.), The Neurosciences: 4th Study Program, MIT Press, Boston, 1979, pp. 617 622. 8 Matthews, H.R., Murphy, R.L.W., Faint, G.L. and Lamb, T.D., Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration, Nature (Lond.), 334 (1988) 67~9. 9 Moore, M.J. and Caspary, D.M., Strychnine blocks binaural inhibition in lateral superior olivary neurons, J. Neurosci., 3 (1983) 237 242. 10 Morest, D.K., The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle, Brain Res., 9 (1968) 288-31 I. 11 Saint-Marie, R.L., Ostapoff0 E.M., Morest, D.K. and Wenthold, R. J., Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance, J. Comp. Neurol., 279 (1989) 382-396. 12 Sans, A., Etchecopar, B., Brehier, A. and Thomasset, M., Immunocytochemical detection of vitamin D-dependent calcium-binding protein (CaBP-28K) in vestibular sensory hair cells and vestibular ganglion neurones of the cat, Brain Res., 364 (1986) 190-194. 13 Sullivan, W.E. and Konishi, M., Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl, J. Neurosci., 4 (1984) 1787-1799. 14 Sullivan, W.E. and Konishi, M., A map of interaural phase differences in the owl's brainstem, Proc. Natl. Acad. Sci. U.S.A., 83 (1986) 8400-8404. 15 Takahashi, T.T., Carr, C.E., Brecha, N. and Konishi, M., Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl, J. Neurosci., 6 (1987) 1843-1856. 16 Thomasset, M., Parkes, C.O. and Cuisinier-Gleizes, P., Rat calcium-binding proteins distribution, ontogen) and vitamin D-dependence, Am. J. Physiol., 243 (1982) E483-E488. 17 Thomasset, M., Desplan, C. and Parkes, C.D., Rat vitamin D-dependent calcium-binding proteins. Specificity of mRNAs coding for the 7,500-Mr protein and the 28,000-Mr protein from kidney and cerebellum, Eur. J. Biochem., 129 (1983) 519 524. 18 Wenthold, R.J., Huie, D., Altschuler, R.A. and Reeks, K.A., Glycine immunoreactivity localized in the cochlear nucleus and the superior olivary complex, Neuroscience, 22 (1987) 897-912.
Neuroscience Letters, 111 (1990) 252 257 Elsevier ScientificPublishers Ireland Ltd.
NSL 06769
Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat W.R. Webster l, C. Batini l, C. Buisseret-Delmas l, C.
C o m p o i n t l,
M. G u e g a n I a n d M. T h o m a s s e t 2 ILahoratoire de Physiologie de la Motrkit~;, CNRS URA 385, Universit~ Pierre et Marie Curie, Paris (France) and~'INSERM, U 120, Le Vesinet (France)
(Received 27 July 1989: Revised version received 29 November 1989: Accepted 1 December 1989) Key word~: Calbindin: 7-Aminobutyricacid: Nucleus trapezoid body: Colocalization Using immunocytochemical methods, both calbindin and GABA were found to be colocalized in the somas of all the cells of the medial nucleus of the trapezoid body (NMTB) of the rat auditory system. In the lateral superior olive (LSO), calbindin was also found in the terminals but not in the cells. Some terminal labelling was found in the medial superior olive (MSO). GABA was also found in the somas of some cells in both LSO and MSO, but most of the labelling was in terminals. In the rat, calbindin appears to be more involved in a pathway that detects interaural intensity differences.
Ca 2 + ions play a key role in the operation of a variety of central nervous system mechanisms, including the release of t r a n s m i t t e r a n d h o r m o n e s [7] a n d light adaptation in rods and cones [8]. They may also be involved in m e m o r y [4]. Inflowing Ca 2+ ions appear to bind to intracellular C a - b i n d i n g proteins such as calbindin, a 28 k D a vitamin D-induced c a l c i u m - b i n d i n g protein [6]. Konishi and his coworkers [15] have argued that the d i s t r i b u t i o n of such e n d o g e n o u s c a l c i u m - b i n d i n g proteins can provide much i n f o r m a t i o n a b o u t the o r g a n i z a t i o n of the brain, but their explicit functional role remains unclear. Konishi and his colleagues [(5] have proposed a challenging functional correlation between the d i s t r i b u t i o n of c a l b i n d i n a n d phaselocking of cells in the a u d i t o r y system of the b a r n owl ( T y t o alba). They used i m m u nocytochemical techniques to show that calbindin is m a i n l y localized to an a u d i t o r y pathway which is involved in phase-locking for the detection of differences in the timing of sounds arriving at the two ears [13, 14]. A n interaural intensity detecting pathway was not labelled with calbindin [15]. T a k a h a s h i et al. [15] do point out that there has been no detailed study of the distri-
Corre,7)ondence: W.R. Webster, Laboratoire de Physiologiede la Motricit6, CNRS URA 385, Universit6 Pierre et Marie Curie, Paris, France.
0304-3940/90/S 03.50 ~ 1990ElsevierScientificPublishers Ireland Ltd.
253 bution of calbindin in the central mammalian auditory system, which could provide a test of the generality of their claim that calbindin is involved in mechanisms that underlie the preservation of the timing of incoming signals in the postsynaptic somata. The present study examined the distribution of calbindin in the rat auditory system and its correlation with that of GABA, which colocalizes with calbindin in the cerebellum [2]. GABA has also been found colocalized with another calciumbinding protein, parvalbumin (PV), in the rat cerebral cortex and cerebellum [5]. Fourteen rats were perfused intracardiacally with a solution of 4% paraformaldehyde in phosphate buffer (0.1 M; pH 7.4) and their brains removed. Free-floating, 40-/~m-thick vibratome sections were cut. Sections from 7 animals were incubated overnight with anti-calbindin 28 kDa serum (1:4000 in PBS) raised in rabbits immunized with purified rat kidney calbindin [6]. Antiserum specificity was checked by Ouchterlony double-immunodiffusion, radioimmunoassay [16] and immunoprecipitation [6]. The second incubation was carried out with goat anti-rabbit diluted to 1:200 in PBS for 1 h 30 min. The final incubation was in rabbit PAP (1:400). The calbindin reactive sites were visualized using 0.5% diaminobenzidine (DAB) by incubating with 0.5% DAB, 0.1% H202 in 0.1 M Tris-HCl, pH 7.6 for 15 rain. The other 7 animals were treated for GABA immunocytochemistry using methods already described in detail [3]. Sections from
Fig. I. A: photomicrographof the rat superior olivarycomplex showingimmunohistochemicallabelling for calbindin. B: enlargement of N M T B at the position of the arrow. C: enlargementof LSO at the position of the arrow.
254
2 GABA and 2 calbindin animals were counterstained for Nisst. Two further animals were perfused and their brains sectioned at 10/~m after paraffin embedding. The sections for one animal was treated for calbindin and those of the other for GABA. Staining for both calbindin and GABA occurred throughout the auditory pathway (the interstitial nucleus of the auditory nerve, the cochlear nuclei, the superior olivary complex, the nuclei of the lateral lemniscus, the inferior colliculus, the medial geniculate body and the auditory cortex). The details of this labelling will be reported later; the present report concentrates on the labelling in the superior olivary complex, as this is the region in the mammalian brain which contains the beginning of both the timing and intensity pathways. In contrast to the finding that calbindin was restricted to a time difference-detecting pathway, we found most calbindin (Fig. I A, B) in the medial nucleus of the trapezoid body (NMTB), which is involved in a pathway for detecting interaural intensity differences [t]. The somata of the cells were labelled in NMTB (Fig. 1A, B). The NMTB has an inhibitory projection to cells of the lateral superior olive (LSO) which are sensitive to interaural intensity differences of high frequency sounds [1]. There is also considerable labelling in the LSO but it is largely confined to terminals surrounding unstained somata (Fig. IA, C). The medial super-
2,
Fig. 2. A: photomicrograph of the rat superior olivary complex showing immunohistochemical labelling for GABA. B: enlargement of labelling at position of solid arrow in NMTB. C: enlargement of labelling at position of open arrow in LSO.
255
ior olive (MSO) is the first site for detecting interaural timing differences of low frequency sounds in the mammalian brain but unlike N M T B no somata were labelled. Like LSO, MSO has only terminals labelled but to a lesser extent (Fig. IA). It is only in N M T B that the somata of cells are clearly labelled for calbindin in the superior olive. The pattern of GABA immunoreactivity in the superior olive was similar in some respects to the calbindin pattern. All the cell somata were GABA-positive in N M T B (Fig. 2A, B). The proportion of GABA and calbindin labelling was checked by counting the number of stained cells in the N M T B before and after counterstaining for Nissl. The same number of cells were observed before and after counterstaining and no cells were found which were stained for Nissl but not for the antibody, therefore it can be concluded that calbindin and GABA are colocalized in the cells of NMTB. The labelling patterns for calbindin and GABA in other parts of the superior olivary complex were different. In the LSO, the somata of several cells were GABA-positive and the labelling also involved terminals around stained and unstained somata (Fig. 2A, C). GABA labelling in the MSO was similar to that of the LSO (Fig. 2A). For all of the superior olive, the same pattern of labelling was seen with 10/tm sections as that found in all the animals with 40/zm sections. This is illustrated in Fig. 3A, in which cells in N M T B are labelled with calbindin and in Fig. 3B where they are labelled with GABA, thus confirming similar results obtained with 40/zm sections. The results of these experiments indicate that the distribution of calbindin in the auditory system of the rat is different from that of the barn owl [15]. Calbindin is not restricted to a pathway involved in the detection of interaural time differences. It appears to be more closely involved in a pathway that detects interaural intensity differences, and which is not labelled for calbindin in the barn owl [15]. While the rat system appears to be different to that of the barn owl, it is not possible to conclude that calbindin is not involved in the time pathway as there is some terminal
Fig. 3. A: photomicrograph of a 10/lm section showing immunocytochemical labelling for calbindin m NMTB. B: a photomicrograph of a 10/Jm section showing immunocytochemical labelling for GABA.
256
labelling in MSO, but it is clear that calbindin is more heavily localized in the intensity pathway. Takahashi et al. [15] have also suggested that calbindin might be associated with the tonic release of neurotransmitter. Sans et al. [12] have shown that calbindin is localized in the vestibular Type II hair cells which have a high tonic rate of firing. Type I hair cells, which fire irregularly, are only weakly immunoreactive. If this were the sole function for calbindin, most of the cells in MSO and LSO should be heavily labelled because when they are excited they tend to fire in a sustained tonic manner [1]. Perhaps the most significant finding in the present study is that calbindin is colocalized with GABA in the cells of NMTB, just as calbindin and GABA are colocalized in the Purkinje cells of the cerebellum [2]. Calbindin, in both instances, may be involved in the release of this inhibitory transmitter. Celio [5] has also shown that GABA and PV are colocalized in the rat cerebellum, and suggests that calcium-binding proteins support the 3 characteristics of GABA neurons: high firing rate, high metabolic activity and receiving mainly excitatory afferents which dominate the dendritic and somatic surface thus allowing GABA neurons to be electrically and metabolically more active than their companion neurons [5]. However, many neurons in the auditory system fire at high rates but they contain neither GABA nor calbindin (for example most of the cells in LSO and MSO in the present study). The high concentration of this calcium-binding protein in the GABA cells of N M T B may be due to the presence and activity of the inhibitory transmitter GABA itself. However, the work of Moore and Caspary [9] on binaural inhibition in the LSO of the chinchilla does not entirely support this suggestion. They tbund that both GABA and glycine could mimic binaural inhibition in LSO, but that only a glycine antagonist and not a GABA antagonist blocked this effect. They concluded that inhibition in LSO arising from cells in NMTB was glycinergic rather than GABAergic. However, as all the cells in rat N M T B contained GABA, the cells projecting to LSO must also contain GABA. The principal cell of N M T B is innervated by a very large synapse (Calyce of Held) and it is these cells which provide the inhibitory projection to LSO. It should be pointed out that the published evidence for this projection comes from work on the cat [1], but unpublished HRP studies of rat N M T B from this laboratory confirm this general projection. Another possibility is that the principal cells of NMTB contain glycine as well as GABA and calbindin. In the cat, cells in NMTB are strongly immunoreactive for glycine [11, 18] but neither study reported labelling for GABA. Further studies on the role of glycine in the rat N M T B are required to clarify the relationship between GABA, glycine and calbindin. 1 Aitkin, L.M., trvine, D.R.F. and Webster W.R.. Central neural mechanisms of hearing. In I. DarianSmith (Ed.), Handbook of Physiology, Section 1: The Nervous System, Vol. 3, Sensory Processes, ch. 16, American Physiological Society, Bethesda, 1984, pp. 675 737. 2 Batini, C., Cerebellar localization and cotocalization of GABA and calcium binding protein vitamin [)-dependent 28 Kd, Arch. ltal. Biol., in press. 3 Batini, C., Buisseret-Delmas, C., Compoint, C. and Daniel, H., The GABAergic neurones of the cerebellar nuclei in the rat: projections to the cerebellar cortex, Neurosci. Lett., 99 (1989) 251 256.
257 4 Brown, T.H., Chapman, P.F., Kairiss, E.W. and Keenan, C.L., Long-term synaptic potentiation, Science, 242 (1988) 724-728. 5 Celio, M.R., Parvalbumin in most y-aminobutyric acid-containing neurons of the rat cerebral cortex, Science, 231 (1986) 995-997. 6 Intrator, S., Elion, J., Thomasset, M. and Brehier, A., Purification, immunological and biochemical characterization of rat 28-K Da cholecalcin (cholecalciferol-induced CaBP's): identity between renal and cerebellar cholecalcins, Biochem. J., 231 (I 985) 89-95. 7 Kretsinger, R.H., Calcium in neurobiology: a general theory of function and evolution. In F.O. Schmitt and F.G. Worden (Eds.), The Neurosciences: 4th Study Program, MIT Press, Boston, 1979, pp. 617 622. 8 Matthews, H.R., Murphy, R.L.W., Faint, G.L. and Lamb, T.D., Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration, Nature (Lond.), 334 (1988) 67~9. 9 Moore, M.J. and Caspary, D.M., Strychnine blocks binaural inhibition in lateral superior olivary neurons, J. Neurosci., 3 (1983) 237 242. 10 Morest, D.K., The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle, Brain Res., 9 (1968) 288-31 I. 11 Saint-Marie, R.L., Ostapoff0 E.M., Morest, D.K. and Wenthold, R. J., Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance, J. Comp. Neurol., 279 (1989) 382-396. 12 Sans, A., Etchecopar, B., Brehier, A. and Thomasset, M., Immunocytochemical detection of vitamin D-dependent calcium-binding protein (CaBP-28K) in vestibular sensory hair cells and vestibular ganglion neurones of the cat, Brain Res., 364 (1986) 190-194. 13 Sullivan, W.E. and Konishi, M., Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl, J. Neurosci., 4 (1984) 1787-1799. 14 Sullivan, W.E. and Konishi, M., A map of interaural phase differences in the owl's brainstem, Proc. Natl. Acad. Sci. U.S.A., 83 (1986) 8400-8404. 15 Takahashi, T.T., Carr, C.E., Brecha, N. and Konishi, M., Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl, J. Neurosci., 6 (1987) 1843-1856. 16 Thomasset, M., Parkes, C.O. and Cuisinier-Gleizes, P., Rat calcium-binding proteins distribution, ontogen) and vitamin D-dependence, Am. J. Physiol., 243 (1982) E483-E488. 17 Thomasset, M., Desplan, C. and Parkes, C.D., Rat vitamin D-dependent calcium-binding proteins. Specificity of mRNAs coding for the 7,500-Mr protein and the 28,000-Mr protein from kidney and cerebellum, Eur. J. Biochem., 129 (1983) 519 524. 18 Wenthold, R.J., Huie, D., Altschuler, R.A. and Reeks, K.A., Glycine immunoreactivity localized in the cochlear nucleus and the superior olivary complex, Neuroscience, 22 (1987) 897-912.
