Peripheral maps and synapse elimination in the cerebellum of the rat. II. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of X-irradiated adult rats

doi:10.1016/0006-8993(87)91291-1

Brain Research

Volume 421, Issues 1–2, 22 September 1987, Pages 211-225

https://doi.org/10.1016/0006-8993(87)91291-1 Get rights and content

Abstract

The present study gives a detailed description of the functional characteristics and of the topographic distribution of responses mediated through the climbing fiber (CF) pathway in the cerebellum of adult rats which have been repeatedly irradiated from birth so that the Purkinje cells (PCs) in the adult remained innervated by several climbing fibers instead of one. Experiments were carried out under urethane anaesthesia. After electrical stimulation of the contralateral snout, the ipsilateral and contralateral hindlimb or forepad, and the tail, CF-EPSPs were recorded from PCs in an area extending 1000 μm laterally to the midline in the vermal part of lobules VII and VIII. The stepwise variation of CF-EPSP amplitude demonstrated the multiple innervation of the PCs by CFs in these animals. The responses of a given PC through separate CFs were analyzed separately and, using precise micromapping techniques and computer analysis, cells were located on the map of the unfolded PC layer. Taking into account the mean latency of the responses and the probability of discharge of the PCs, restricted areas of projection were found for the snout, the forepads and the tail. Zones of short-latency responses formed compact patches of approximately 1 mm². Their disposition was very similar to that found in normal rats. The responses evoked through the different CFs converging on a given PC were in general very homogeneous and very similar to those recorded in control rats. There was some overlap of projection zones from tail and snout and from forepads and snout. In this latter case, there was a convergence of several peripheral inputs on some of the PCs tested. No precise projection of the hindlimbs could be detected in the same lobules. These results suggest that, with the type of stimulation used, the representation of peripheral inputs through CF pathway is roughly conserved even though multiple innervation of PCs by CFs is maintained until adulthood.

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Cited by (14)

A Model of Developmental Synapse Elimination in the Central Nervous System: Possible Mechanisms and Functional Consequences
1997, Advances in Organ Biology
Recent research into the developmental elimination of supernumerary synapses has increased understanding of this process. We discuss in this chapter synapse elimination both at the neuromuscular junction and in the central nervous system, in terms of some possible underlying mechanisms suggested by recent studies. A well-characterized example of central nervous system synapse elimination, the climbing fiber-Purkinje cell synapse of the cerebellum, is used to explore the functional significance of synaptic regression during development.
Abnormal ipsilateral functional vibrissae projection onto Purkinje cells multiply innervated by climbing fibers in the rat
1995, Developmental Brain Research
We have previously shown that synapse elimination occurring in the climbing fiber (CF)-Purkinje cell (PC) relationships during normal postnatal development is likely involved in the refinement of vibrissae projections onto the cerebellar cortex. In normal adult rats, CF-mediated vibrissae projections onto cerebellar Purkinje cells of the vermis of lobule VII are strictly contralateral and located in a narrow microzone whereas they are widely distributed in rats whose PCs remained multiply innervated by CFs due to postnatal irradiation. Given the proximity of this microzone to the midline, the question arose as to whether this synapse elimination process could participate in the segregation of ipsilateral and contralateral projections. In the present study, we compared the topographical map of the ipsilateral and contralateral CF-mediated projections of the third row of vibrissae onto the vermal PCs of lobule VII in adult normal rats and in polyinnervated rats. Using intracellular electrophysiological recordings, we examined the responsiveness of PCs to mechanical stimulation of vibrissae, and positioned responsive cells on an averaged planar map of lobule VII. In normal rats no ipsilateral responses were found, while in irradiated rats ipsilateral responses were distributed evenly from the midline to 700 μm apart. These results suggest that synapse elimination participates in the segregation of ipsi and contralateral mystacial inputs to the vermis.
Enlargement of olivo-cerebellar microzones in the agranular cerebellum of adult rats
1994, Brain Research
Previous work on normal adult rat showed that the vibrissae project, through the climbing fiber (CF) system, onto the Purkinje cells (PCs) of the contralateral cerebellar hemivermis of lobule VII. The highly elaborated CF projections from a given row of vibrissae delimit a narrow parasagittal zone which can be regarded as a functional olivo-cerebellar microzone. Interestingly, the adult one-to-one relationship between PCs and CFs is preceded by a transient phase during which each PC receives synaptic inputs from several CF collaterals which will be eliminated but one, when granule cells begin to establish synapses on PCs. Therefore, the question arose as to whether this synaptic elimination process could participate in the refinement of the topographical organization of CF projections and could contribute to the formation of such precise peripheral maps onto the cerebellum. In the present study, the topographical map of the CF-mediated projections of mystacial vibrissae onto the vermal PCs of lobule VII was determined in adult rats whose cerebellar PCs remain polyinnervated by olivary CFs due to degranulation by postnatal X-irradiation. Using intracellular recordings, we examined the responsiveness of PCs in lobule VII during mechanical stimulation of the 3rd row of contralateral vibrissae, and positioned cells responding to the stimulation on an averaged planar map of lobule VII. Comparison of the results to those obtained in our previous work on normal rats showed that the activated cells were more numerous and more diffusely distributed. PCs exhibiting the best characteristics of response were distributed evenly from the midline to 700 μm lateral in the contralateral hemivermis and not gathered in a parasagittal microzone centered on the plane 200 μm as in normal rats. These results strongly suggest that synaptic elimination in the olivo-cerebellar system participates in the segregation of CF-mediated inputs into functional microzones on the cerebellar cortex.
Extent of multiple innervation of cerebellar Purkinje cells by climbing fibers in adult X-irradiated rats. Comparison of different schedules of irradiation during the first postnatal week
1990, Developmental Brain Research
The multiple innervation of cerebellar Purkinje cells (PCs) by climbing fibers (CFs) that is transient in normal developing rats can be experimentally maintained in cerebella which have been degranulated by repetitive postnatal X-irradiation restricted to the first postnatal week²². Since the involution of redundant CFs occurs essentially between postnatal days 5 and 10, and given that postirradiation effects last 2–3 days, the question arose to know whether it is possible to further delimit a ‘critical period’ of irradiation within the first week. An estimate of the extent of multiple innervation of PCs by CFs was made in adult rats that had been irradiated according to 5 different schedules: in two groups, rats received X-rays applied repetitively during the first postnatal week (PN0–7 groups); in the 3 other groups, X-rays were delivered either during the first part of the week (early group PN1–3) or during the last part of the week (late groups PN4–7). In addition, two daily doses were tested (150 and 200 r). The CF pathway was electrically stimulated in anesthetized rats at the level of the inferior olive or in the cerebellar white matter. Intracellular recordings of spontaneous and evoked CF responses in PCs allowed to estimate the number of afferent CFs and to calculate the mean value (m) per PC for each group. The majority of recorded cells was located in lobules VII and VIII and similar results were obtained in these two lobules. In lobule VII, irradiation restricted to the first part of the week (early group) did not impede most of the regression (m = 1.27 ± 0.06). In contrast, high doses (200 r) applied during the second part of the week (late group) maintained a high index of multiple (m = 3.05 ± 0.05) innervation, very close to the level obtained in the 0–7 group receiving similar doses on corresponding days (m = 3.32 ± 0.07). Homologous groups receiving the lower daily dose (150 r) maintained a significantly lower index of multiple innervation.
Representation of vibrissae inputs through the climbing fiber pathway in lobule VII of the adult rat cerebellar vermis
1989, Brain Research
The present study gives a detailed description of the functional characteristics and of the topographic distribution of Purkinje cell (PC) responses, mediated through the climbing fiber pathway and elicited by mechanical stimulation of two different rows (A and C) of vibrissae in a circumscribed region of the posterior vermis of the rat cerebellum. Experiments were carried out on normal adult rats under barbiturate anethesia. PCs were recorded in an area extending 1500 μm laterally to the midline in the vermal part of lobule VII contralateral to the stimulation. Using micromapping techniques and computer analysis, we located the cells on the map of the unfolded PC layer. Taking into account the mean latency of the responses and the probability of discharge of PCs, restricted areas of projection were found. For each row, these areas formed two longitudinal patches located between midline and plane 1100 μm and separated by a non-responsive plane at 500 μm. Cells having the best characteristics of responses to the stimulation of row C were located mainly in plane 200 μm. Cells giving the best responses to the stimulation of row A were located mainly in the posterior part of plane 200 μm which was therefore a zone of convergence for both rows.
Peripheral maps and synapse elimination in the cerebellum of the rat.I. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of the normal adult rat
1987, Brain Research
The present study gives a detailed description of the functional characteristics and of the topographic distribution of responses, mediated through the climbing fiber pathway and elicited by electrical stimulation of several peripheral inputs, in a circumscribed region of the posterior vermis of the rat cerebellum. Experiments were carried out on normal adult rats under urethane anaesthesia. Purkinje cells (PCs) which responded to the electric stimulation of the contralateral snout, of the ipsilateral and contralateral hindlimb or forepad, and of the tail were recorded in an area extending 1000 μm laterally to the midline in the vermal part of lobules VII and VIII. Using precise micromapping techniques and computer analysis, we located the cells on the map of the unfolded PC layer. Taking into account the mean latency of the responses and the probability of discharge of the PCs, restricted areas of projection were found for the snout, the forepads and the tail. Zones of short-latency responses form compact patches of less than 1 mm². There was some overlap of projection zones from tail and snout and from forepads and snout. In these zones, there was a convergence of several peripheral inputs on some of the PCs tested. No precise projection of the hindlimbs could be detected in the same lobules. These results fit well with the hypothesis already proposed that the representation of peripheral inputs through the climbing fiber pathway is fractured into a mosaic of patches, which are partly overlapping, and in which remote parts of the body are represented in adjacent areas.

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Peripheral maps and synapse elimination in the cerebellum of the rat. II. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of X-irradiated adult rats

Abstract

Dev. Brain Res.

Dev. Brain Res.

Neurosci. Lett.

J. Neurobiol.

Creation of a data base to process neurophysiological results obtained in the cerebellum

Postnatal development of the cerebellar cortex in the rat

J. Comp. Neurol.

Morphological development of the rat cerebellum and some of its mechanisms

Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged X-irradiation started at birth

J. Comp. Neurol.

Experimental reorganization of the cerebellar cortex. II. Effects of elimination of most microneurons with prolonged X-irradiation started at four days

J. Comp. Neurol.

Prenatal development of the cerebellar system in the rat

J. Comp. Neurol.