Molecular, Topographic, and Functional Organization of the Cerebellar Cortex: A Study with Combined Aldolase C and Olivocerebellar Labeling

Sugihara, Izumi; Shinoda, Yoshikazu

doi:10.1523/jneurosci.1961-04.2004

Cited by 274 publications

(496 citation statements)

References 53 publications

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“…Specifically, the regional variation in synchrony loss (Fig. 5), combined with the fact that climbing fiber projections to crus 2a arise from multiple IO regions (Buisseret-Delmas and Angaut, 1993;Sugihara and Shinoda, 2004), suggest that diffusion barriers were a major reason for the incomplete loss of synchrony. Another factor is that carbenoxolone does not completely block electrical coupling (Rozental et al, 2001), as confirmed by the climbing fiber reflex results.…”

Section: Gap Junction Coupling Between Io Neurons Mediates Cs Synchronymentioning

confidence: 99%

“…To test this possibility, we made use of the fact that each region of the rat IO projects to a narrow rostrocaudally oriented strip of cortex (Buisseret-Delmas and Angaut, 1993;Sugihara and Shinoda, 2004), which corresponds to approximately two to three columns of cells in the recording array. Because we did not know the actual borders of the projection zones, we used a sliding window of three columns (Fig.…”

Section: Intercell Variation Of the Effect Of Carbenoxolone On Cs Synmentioning

confidence: 99%

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Block of Inferior Olive Gap Junctional Coupling Decreases Purkinje Cell Complex Spike Synchrony and Rhythmicity

2006

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Inferior olivary (IO) neurons are electrotonically coupled by gap junctions. This coupling is thought to underlie synchronous complex spike (CS) activity generated by the olivocerebellar system in Purkinje cells, and also has been hypothesized to be necessary for IO neurons to generate spontaneous oscillatory activity. These characteristics of olivocerebellar activity have been proposed to be central to the role of this system in motor coordination. However, the relationship of gap junction coupling between IO neurons to synchronous and rhythmic CS activity has never been directly tested. Thus, to address this issue, multiple electrode recordings were obtained from crus 2a Purkinje cells, and carbenoxolone, a gap junction blocker, was injected into the IO. Carbenoxolone reduced CS synchrony by 50% overall, but in some experiments, Ͼ80% reductions were achieved. Carbenoxolone also reduced the average firing rate by 50%, suggesting that electrical coupling is a significant source of excitation for IO neurons. Moreover, carbenoxolone caused a reduction in the ϳ10 Hz rhythmicity of CS activity, and this reduction was correlated with the extent to which the injection reduced CS synchrony. Lastly, carbenoxolone was found to reverse or prevent changes in synchrony that are normally induced by injection of GABA A and glutamate receptor antagonists into the IO, suggesting that the effects of these drugs on CS synchrony patterns require electrical coupling of IO neurons. In sum, our results provide direct evidence that electrical coupling of IO neurons underlies synchronous CS activity, and suggest important roles for this coupling in shaping other aspects of IO spiking patterns.

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Section: Gap Junction Coupling Between Io Neurons Mediates Cs Synchronymentioning

confidence: 99%

Section: Intercell Variation Of the Effect Of Carbenoxolone On Cs Synmentioning

confidence: 99%

Block of Inferior Olive Gap Junctional Coupling Decreases Purkinje Cell Complex Spike Synchrony and Rhythmicity

2006

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“…Seven aldolase C-positive (1ϩ to 7ϩ) and -negative (1Ϫ to 7Ϫ) compartments are known to exist in each hemicerebellum (Brochu et al, 1990). PCs in each aldolase C compartment receive projections from neurons located in specific subnuclei of the inferior olive (Sugihara and Shinoda, 2004). PCs in each aldolase C compartment in turn project to a distinct subdivision of the deep cerebellar nuclei (Sugihara, 2011), which sends inhibitory projections back to the inferior olive (de Zeeuw et al, 1989).…”

Section: Introductionmentioning

confidence: 99%

Structure–Function Relationships between Aldolase C/Zebrin II Expression and Complex Spike Synchrony in the Cerebellum

et al. 2015

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Simple and regular anatomical structure is a hallmark of the cerebellar cortex. Parasagittally arrayed alternate expression of aldolase C/zebrin II in Purkinje cells (PCs) has been extensively studied, but surprisingly little is known about its functional significance. Here we found a precise structure-function relationship between aldolase C expression and synchrony of PC complex spike activities that reflect climbing fiber inputs to PCs. We performed two-photon calcium imaging in transgenic mice in which aldolase C compartments can be visualized in vivo, and identified highly synchronous complex spike activities among aldolase C-positive or aldolase C-negative PCs, but not across these populations. The boundary of aldolase C compartments corresponded to that of complex spike synchrony at single-cell resolution. Sensory stimulation evoked aldolase C compartment-specific complex spike responses and synchrony. This result further revealed the structure-function segregation. In awake animals, complex spike synchrony both within and between PC populations across the aldolase C boundary were enhanced in response to sensory stimuli, in a way that two functionally distinct PC ensembles are coactivated. These results suggest that PC populations characterized by aldolase C expression precisely represent distinct functional units of the cerebellar cortex, and these functional units can cooperate to process sensory information in awake animals.

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“…Neurons from specific parts of the inferior olive send their climbing fibers to narrow, longitudinally arranged, strips of Purkinje cells (Voogd and Glickstein, 1998;Sugihara and Shinoda, 2004). These strips of Purkinje cells project to specific regions of the cerebellar nuclei that also receive direct input from collaterals of the same climbing fibers, thus resulting in a modular arrangement of olivo-cortico-nuclear connections (Pijpers et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…In the figures, roman numerals indicate individual lobules, and arrows are used to indicate their apices. The zebrin-positive bands are presented in gray, and the numbers and letters in these bands refer to the zebrinpositive compartments as defined by Hawkes and Leclerc (1987) and modified by Voogd and Ruigrok (2004) and by Sugihara and Shinoda (2004). The corresponding negative bands are positioned directly lateral to the positive bands.…”

Section: Introductionmentioning

confidence: 99%

Precise Spatial Relationships between Mossy Fibers and Climbing Fibers in Rat Cerebellar Cortical Zones

Pijpers¹,

Apps²,

Pardoe³

et al. 2006

J. Neurosci.

126

132

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Classically, mossy fiber and climbing fiber terminals are regarded as having very different spatial distributions in the cerebellar cortex. However, previous anatomical studies have not studied these two major cerebellar inputs with sufficient resolution to confirm this assumption. Here, we examine the detailed pattern of collateralization of both types of cerebellar afferent using small injections of the bidirectional tracer cholera toxin b subunit into the posterior cerebellum. The cortical and zonal location of these injections was characterized by mapping climbing fiber field potentials, the distribution of retrogradely labeled olivary neurons, and the intrinsic zebrin pattern of Purkinje cells.Labeled climbing fiber collaterals were distributed as longitudinal strips and were always accompanied by clusters of labeled mossy fiber rosettes in the subjacent granular layer. Two-and three-dimensional reconstructions and quantitative analysis showed that mossy fibers also collateralized to other stripe-like regions usually below Purkinje cells with the same zebrin-positive or zebrin-negative characteristics as that of the injection site and associated climbing fiber collaterals. The distribution of retrogradely labeled neurons in two major sources of mossy fibers, the lateral reticular and basilar pontine nuclei, revealed interlobular and some interzonal differences.These data indicate that nonadjacent cerebellar zones, sharing the same climbing fiber input and zebrin identity, also share a common mossy fiber input. Other cerebellar cortical regions that receive collaterals from the same mossy fibers usually also have the same zebrin signature. Together with the distribution of neurons in precerebellar centers, the findings suggest a revision of the modular hypothesis for information processing in the cerebellar cortex.

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Molecular, Topographic, and Functional Organization of the Cerebellar Cortex: A Study with Combined Aldolase C and Olivocerebellar Labeling

Cited by 274 publications

References 53 publications

Block of Inferior Olive Gap Junctional Coupling Decreases Purkinje Cell Complex Spike Synchrony and Rhythmicity

Block of Inferior Olive Gap Junctional Coupling Decreases Purkinje Cell Complex Spike Synchrony and Rhythmicity

Structure–Function Relationships between Aldolase C/Zebrin II Expression and Complex Spike Synchrony in the Cerebellum

Precise Spatial Relationships between Mossy Fibers and Climbing Fibers in Rat Cerebellar Cortical Zones

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