Maturation of climbing fiber responses in the rat

Crépel, F.

doi:10.1016/0006-8993(71)90617-2

Cited by 123 publications

(43 citation statements)

References 6 publications

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“…A previous study of olivocerebellar conduction time to the vermis showed that CS response latencies following IO stimulation dropped steadily from a high at P4 until they leveled off around P22 (Crepel 1971). Our results are generally consistent with this prior study in showing a rapid decline in evoked CS latency from P14 to P25.…”

Section: Both Myelin and Nonmyelin Related Factors Shape Olivocerebelsupporting

confidence: 92%

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

Lang¹,

Rosenbluth

2003

Journal of Neurophysiology

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Lang, Eric J. and Jack Rosenbluth. Role of myelination in the development of a uniform olivocerebellar conduction time. J Neurophysiol 89: 2259 -2270, 2003. First published December 18, 2002 10.1152/jn.00922.2002. Purkinje cells generate simultaneous complex spikes as a result of olivocerebellar activity. This synchronization (to within 1 ms) is thought to result from electrotonic coupling of inferior olivary neurons. However, the distance from the inferior olive (IO) varies across the cerebellar cortex. Thus signals generated simultaneously at the IO should arrive asynchronously across the cerebellar cortex, unless the length differences are compensated for. Previously, it was shown that the conduction time from the IO to the cerebellar cortex remains nearly constant at Ϸ4 ms in the rat, implying the existence of such compensatory mechanisms. Here, we examined the role of myelination in generating a constant olivocerebellar conduction time by investigating the latency of complex spikes evoked by IO stimulation during development in normal rats and myelin-deficient mutants. In normal rats, myelination not only reduced overall olivocerebellar conduction time, but also disproportionately reduced the conduction time to vermal lobules, which had the longest response latencies prior to myelination. The net result was a nearly uniform conduction time. In contrast, in myelin-deficient rats, conduction time differences to different parts of the cerebellum remained during the same developmental period. Thus myelination is the primary factor in generating a uniform olivocerebellar conduction time. To test the importance of a uniform conduction time for generating synchronous complex spike activity, multiple electrode recordings were obtained from normal and myelin-deficient rats. Average synchrony levels were higher in normal rats than mutants. Thus the uniform conduction time achieved through myelination of olivocerebellar fibers appears to be essential for the normal expression of complex spike synchrony. I N T R O D U C T I O NInferior olivary (IO) neurons are electrotonically coupled via numerous gap junctions (Llinás and Yarom 1981;Llinás et al. 1974;Sotelo et al. 1974). Indeed, the density of neuronal gap junctions appears to be higher in the IO than in any other CNS region (Belluardo et al. 2000;Condorelli et al. 1998;De Zeeuw et al. 1995). This coupling allows IO neurons to generate precisely (on a millisecond time scale) synchronized activity that results in simultaneous complex spike (CS) activity in the cerebellum (Lang et al. 1999;Sasaki et al. 1989;Sugihara et al. 1993;Yamamoto et al. 2001).Maintenance of the synchronization present in IO discharges presents a challenge for the olivocerebellar system because the length of the olivocerebellar pathway to different points on the cerebellar cortex varies. In rats, there can be more than a twofold difference in the length of the olivocerebellar projection to different regions of the cortex (Sugihara et al. 1993). To preserve the precise synchronization present at...

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Section: Both Myelin and Nonmyelin Related Factors Shape Olivocerebelsupporting

confidence: 92%

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

Lang¹,

Rosenbluth

2003

Journal of Neurophysiology

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“…Previous in vivo studies have also followed developing Purkinje cells, showing that complex spike activity can be detected during the first week after birth in rats (Crepel 1971;Shimono et al 1976;Sokoloff et al 2014;Woodward et al 1969). More recently, whole cell in vivo electrophysiology conducted in developing mice also demonstrated complex spike activity in the first week of life (Kawamura et al 2013).…”

Section: Discussionmentioning

confidence: 96%

In vivo analysis of Purkinje cell firing properties during postnatal mouse development

Arancillo

White

Lin

et al. 2015

Journal of Neurophysiology

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Arancillo M, White JJ, Lin T, Stay TL, Sillitoe RV. In vivo analysis of Purkinje cell firing properties during postnatal mouse development. J Neurophysiol 113: 578 -591, 2015. First published October 29, 2014 doi:10.1152/jn.00586.2014.-Purkinje cell activity is essential for controlling motor behavior. During motor behavior Purkinje cells fire two types of action potentials: simple spikes that are generated intrinsically and complex spikes that are induced by climbing fiber inputs. Although the functions of these spikes are becoming clear, how they are established is still poorly understood. Here, we used in vivo electrophysiology approaches conducted in anesthetized and awake mice to record Purkinje cell activity starting from the second postnatal week of development through to adulthood. We found that the rate of complex spike firing increases sharply at 3 wk of age whereas the rate of simple spike firing gradually increases until 4 wk of age. We also found that compared with adult, the pattern of simple spike firing during development is more irregular as the cells tend to fire in bursts that are interrupted by long pauses. The regularity in simple spike firing only reached maturity at 4 wk of age. In contrast, the adult complex spike pattern was already evident by the second week of life, remaining consistent across all ages. Analyses of Purkinje cells in alert behaving mice suggested that the adult patterns are attained more than a week after the completion of key morphogenetic processes such as migration, lamination, and foliation. Purkinje cell activity is therefore dynamically sculpted throughout postnatal development, traversing several critical events that are required for circuit formation. Overall, we show that simple spike and complex spike firing develop with unique developmental trajectories.

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“…However, the appearance of cerebellin also coincides with the entry of climbing fibers into the cerebellum (postpartum days [3][4][5] in rat; refs. 8 and 9) and their formation of cerebellar nests around immature Purkinje cells (8,10,11). Since climbing fibers establish somatic synapses onto Purkinje cells during this period (8,(11)(12)(13) they might also supply a trigger for cerebellin expression.…”

Section: Discussionmentioning

confidence: 99%

“…8 and 9) and their formation of cerebellar nests around immature Purkinje cells (8,10,11). Since climbing fibers establish somatic synapses onto Purkinje cells during this period (8,(11)(12)(13) they might also supply a trigger for cerebellin expression. The rapid rise in cerebellin levels between days 8 and 25 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Cerebellin: a quantifiable marker for Purkinje cell maturation.

Slemmon¹,

Danho²,

Hempstead³

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

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The cerebellum-specific hexadecapeptide cerebellin has been localized by immunocytochemical means to the perikarya and dendrites of cerebellar Purkinje cells. Biochemical analysis using ion-pairing HPLC shows cerebellin to first appear 5 days after birth, whereafter levels rise to a maximum at 25 days postpartum, and then decline to stable adult values. This same pattern of development occurs with a lag of approximately 5 days for the major metabolite of cerebellin, des-Serl-cerebellin. The immunocytochemical picture of cerebellin in developing Purkinje cells mirrors the biochemical data. These results show that cerebellins represent unique quantifiable markers for the investigation of Purkinje cell maturation and lend support to the feasibility of using unique endogenous peptides to chart neurodevelopment.We have proposed that by systematically identifying naturally occurring unique peptides of neural structures these could be used as quantifiable molecular markers with which to investigate neurodevelopment (1). In a prototype study two cerebellum-specific peptides were isolated and sequenced and shown to be a hexadecamer termed cerebellin (NH2-Ser-Gly-Ser-Ala-Lys-Val-Ala-Phe-Ser-Ala-Ile-ArgSer-Thr-Asn-His-OH) and an apparent metabolite des-Serlcerebellin (1). It thus remained to establish the utility of the cerebellins as molecular markers for neurodevelopment and to determine their cellular location. Since both cerebellins have been synthesized (1), we have been able to develop antibodies to the peptides that can be used for their localization at the level of the light microscope. Furthermore, as sensitive biochemical analysis of the peptides is possible (1), immunocytochemical evidence could be corroborated and quantitated in adult and developing cerebellum. In this study the immunocytochemical localization of cerebellin in Purkinje cells is reported as well as the characteristics of cerebellin expression during ontogeny. The demonstration of these parameters lends support to the feasibility of using native endogenous peptides to map development in the brain. MATERIALS AND METHODSPreparation of Immunogen. Cerebellin immunogen was synthesized by incubating together 2 mg of cerebellin and 30 mg of bovine thyroglobulin (Sigma) in 2.8 ml of 50 mM sodium phosphate (pH 7.8) containing a final concentration of 0.5% glutaraldehyde for 2 hr at room temperature. The complex was dialyzed against incubation buffer, and then 1-mg aliquots were used to immunize rabbits. Details of the immunization procedures are as previously reported (2).Affinity Purification of Rabbit Antiserum to Cerebeflin. One milliliter of rabbit antiserum (titered by using a cerebellin radioimmunoassay; unpublished data) was passed over a 1-ml protein A-Sepharose column (Pharmacia) under the conditions recommended by the suppliers. The IgG fraction was neutralized with 0.2 vol of 1 M sodium phosphate (pH 7.6) and passed over a 1-ml cerebellin-agarose affinity column at a flow rate of 10 ml/hr. After loading, the column was washed with 20 ml...

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Maturation of climbing fiber responses in the rat

Cited by 123 publications

References 6 publications

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

Role of Myelination in the Development of a Uniform Olivocerebellar Conduction Time

In vivo analysis of Purkinje cell firing properties during postnatal mouse development

Cerebellin: a quantifiable marker for Purkinje cell maturation.

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