Electrophysiological Excitability and Parallel Fiber Synaptic Properties of Zebrin-Positive and -Negative Purkinje Cells in Lobule VIII of the Mouse Cerebellar Slice.

Viet T Nguyen-Minh,Khoa Tran-Anh,Izumi Sugihara,Yuanjun Luo

doi:10.3389/fncel.2018.00513

Viet T Nguyen-Minh, Khoa Tran-Anh + Show 2 more

Open Access

https://doi.org/10.3389/fncel.2018.00513

Copy DOI

Abstract

Heterogeneous populations of cerebellar Purkinje cells (PCs) are arranged into separate longitudinal stripes, which have different topographic afferent and efferent axonal connections presumably involved in different functions, and also show different electrophysiological properties in firing pattern and synaptic plasticity. However, whether the differences in molecular expression that define heterogeneous PC populations affect their electrophysiological properties has not been much clarified. Since the expression pattern of many of such molecules, including glutamate transporter EAAT4, replicates that of aldolase C or zebrin II, we recorded from PCs of different “zebrin types” (zebrin-positive = aldolase C-positive = Z+; and Z−) in identified neighboring stripes in vermal lobule VIII, in which Z+ and Z− stripes occupy similar widths, in the Aldoc-Venus mouse cerebellar slice preparation. Regarding basic cellular electrophysiological properties, no significant differences were observed in input resistance or in occurrence probability of types of firing patterns between Z+ and Z− PCs. However, the firing frequency of the tonic firing type was higher in Z− PCs than in Z+ PCs. In the case of parallel fiber (PF)-PC synaptic transmission, no significant differences were observed between Z+ and Z− PCs in interval dependency of paired pulse facilitation or in time course of synaptic current measured without or with the blocker of glutamate receptor desensitization. These results indicate that different expression levels of the molecules that are associated with the zebrin type may affect the intrinsic firing property of PCs but not directly affect the basic electrophysiological properties of PF-PC synaptic transmission significantly in lobule VIII. The results suggest that the zebrin types of PCs in lobule VIII is linked with some intrinsic electrophysiological neuronal characteristics which affect the firing frequency of PCs. However, the results also suggest that the molecular expression differences linked with zebrin types of PCs does not much affect basic electrophysiological properties of PF-PC synaptic transmission in a physiological condition in lobule VIII.

Highlights

Purkinje cells (PCs), the sole output neuron of the cerebellar cortex, play an essential role in cerebellar motor and non-motor function through the integration of climbing fiber and parallel fiber (PF) excitatory inputs and inhibitory inputs from molecular layer inhibitory neurons (Ito, 2012)
Besides comparing basic electrophysiological properties of Z+ and Z− PCs, we examined the differences in their PF-PC synaptic transmission, since the EAAT4 expression in PF-PC synapse is linked to the zebrin type and has been implicated in decay of the synaptic current through glutamate uptake (Yamada et al, 1997; Dehnes et al, 1998)
Among 44 PCs recorded in lobule VIII, tonic firing (Figure 2A), initial bursting (Figure 2B) and complex bursting (Figure 2C) types were found in 57% (n = 25), 16% (n = 7) and 27% (n = 12) PCs, respectively

Summary

Introduction

Purkinje cells (PCs), the sole output neuron of the cerebellar cortex, play an essential role in cerebellar motor and non-motor function through the integration of climbing fiber and parallel fiber (PF) excitatory inputs and inhibitory inputs from molecular layer inhibitory neurons (Ito, 2012). The local neuronal circuitry is uniform throughout the cerebellar cortex, PCs are organized into heterogeneous populations based on the expression profile of many molecules, which are distributed in longitudinally-striped patterns in the cerebellar cortex. The striped distribution pattern of heterogeneous populations of PCs is best clarified in the case of zebrin II or glycolytic enzyme aldolase C (Brochu et al, 1990; Fujita et al, 2014). Expression of several molecules, including EAAT4, a neuronal glutamate transporter (Dehnes et al, 1998), exactly matches with that of aldolase C (Dehnes et al, 1998; Hawkes, 2014), high and low in Z+ and Z− PCs (‘‘zebrin type’’), respectively. The functional significance of the different expression profiles of these molecules are barely understood, it may be possible that differences in expression of these molecules affect the physiological properties of individual PCs

Methods

Results

Conclusion