Elsevier

Neuroscience Letters

Volume 705, 13 July 2019, Pages 106-111
Neuroscience Letters

Research article
Temporal-spacial relationships between facial stimulation-evoked filed potential responses in mouse cerebellar granular layer and molecular layer

https://doi.org/10.1016/j.neulet.2019.04.051Get rights and content

Highlights

  • Facial stimulation evoked successively field potentials in cerebellar ML and GL.

  • The field potentials express an excitatory component, N1 and an inhibitory component, P1.

  • Latencies of P1 in both GL and ML were similar regardless the relative recording sites in GL.

  • Blocking either AMPA or GABAA receptors abolished P1 in both ML and GL.

Abstract

The cerebellum receives sensory inputs from mossy fiber-granule cell or climbing fiber pathways, and generates motor-related outputs. However, the temporal and special mechanism of the sensory information processing in cerebellar cortex is still unclear. Therefore, we here investigated the temporal-spacial mechanism between the facial stimulation-evoked field potential responses in granular layer (GL) and molecular layer (ML), by duo-electrophysiological recording technique and pharmacological methods in urethane-anesthetized mice. Our results showed that air-puff stimulation of ipsilateral whisker pad evoked successively field potential responses in GL and ML. The field potential response in GL exhibited a strong excitatory component (N1) followed by an inhibitory component (P1), while the field potential response in ML exhibited a tiny excitatory component (N1) followed by strong inhibitory component (P1). The latency of N1 was decreased with the increase of recording depth in ML, and it was the shortest in GL. Notably, the latencies of P1 in GL and ML were similar regardless the relative recording sites. Furthermore, blocking α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor-mediated parallel fiber excitatory inputs by application of AMPA receptor antagonist, NBQX prevented P1 in both ML and GL. Moreover, application of GABAA receptors antagonist, gabazine simultaneously abolished P1 in both ML and GL. These results indicate that the facial stimulation evoked a simultaneous GABAergic inhibition in both ML and GL via mossy fiber-GC-parallel fiber pathway, suggesting that the sensory stimulation simultaneously evoked excitation of molecular layer interneurons (MLIs) and GL Golgi cells in cerebellar cortex.

Introduction

The cerebellar cortex is organized into three layers: molecular layer (ML), Purkinje cell layer (PCL) and granule cell layer (GL), which is composed mainly of Purkinje cell (PC), granular cells (GC), molecular interneurons (MLIs) and Golgi cells [1]. The PCs are the focus of computation in the cerebellar cortex that receives converging projections from all other cortical neurons and provides the sole output from the cerebellar cortex to the deep cerebellar nuclei. GCs are the most commonly found neurons in the cerebellar cortex; they have the smallest cell somas and short dendrites [1,2]. Golgi cells are inhibitory interneurons of GCs, which are activated by mossy fibers and parallel fibers, and modulate excitatory synaptic transmission through mossy fiber-parallel fiber pathway by offering feed-back inhibition in local GCs [[1], [2], [3], [4]].

MLIs are divided into stellate-type and basket-type MLIs, which receive both excitatory and inhibitory inputs from parallel fibers and other interneurons, and provide GABAergic inhibition to the PCs [[5], [6], [7], [8]]. Stellate-type MILs have been suggested to provide dendritic inhibition and counterbalance parallel fiber excitatory inputs of PCs [9]. Basket-type MLIs offer powerful somatic inhibition of the PC soma and initial segment [8,10,11]. These MLIs exhibit small somas, high-input resistance with a low threshold for activation [12], and are connected with gap-junction, therefore, activating single parallel fiber inputs reliably evokes firing in a MLI, resulting in activation of a group of interneurons through the electric synapses [13,14].

There are two main types of excitatory afferents: the mossy fibers and the climbing fibers, which are considered to transfer the sensory information to cerebellar cortex. They information transferred to PC through the climbing fibers could activate the PCs by firing complex spikes, while the information carried by mossy fibers could excite PCs, MLIs and Golgi cells [5,[15], [16], [17]]. Electrical stimulus of the ML induces excitation followed by rapid activation of feedback inhibition [1,18] and feed forward inhibition in cerebellar PCs [7]. We previously found that sensory stimulation of trigeminal afferents primary induced GABAergic inhibition to PCs but evoked spike firing in both basket-type and stellate-type MLIs via mossy fiber-GC-parallel fiber pathway [19,20,17].

It is clear that during the facial sensory information transferred to cerebellar cortex via mossy fiber-GC-parallel fiber pathway, which induces a sequence of field potential responses in GL and ML. In GL, the sensory information evokes spike firing of GCs, and the action potentials of GCs flow along parallel fibers to excite MLIs, PCs and Golgi cells. Therefore, we assume that the facial information coming from parallel fibers would evoke a simultaneous excitation in MLIs and Golgi cells. For understanding whether the facial stimulation could evoke a simultaneous excitation in MLIs and Golgi cells, we here investigated the temporal-spacial relationships between the facial stimulation-evoked field potential responses in GL and ML, by electrophysiological recording technique and pharmacological methods.

Section snippets

Anesthesia and surgical procedures

Experimental procedures were approved by the Animal Care and Use Committee of Yanbian University and were in accordance with the animal welfare guidelines of the U.S. National Institutes of Health. The permit number is SYXK (Ji) 2011-006. Anesthesia and surgical procedures have been described previously [19]. Either male (n = 12) or female (n = 12) adult (6 to 8-week-old) HA/ICR mice were housed under a 12 h light: 12 h dark cycle with free access to food and water. They were anesthetized with

Due electrophysiological recordings showing the temporal-spacial properties of the facial stimulation-evoked field potential responses in mouse cerebellar GL and ML

For understanding the temporal-spacial properties of facial stimulation-evoked field potential responses in the GL and ML, we first examined the horizon-spacial temporal properties of the facial stimulation-evoked field potential responses in GL and different sites of same depth in ML (Fig. 1A). Under the current-clamp conditions (I = 0), duo-electrophysiological recordings showing that air-puff stimulation (60 ms, 60 psi) on the ipsilateral whisker pad evoked field potential responses in GL

Discussion

The main finding of this study is the facial stimulation evoked simultaneous inhibitory components in GL and ML regardless the relative recording sites. Application of AMPA receptor antagonist, NBQX completely blocked the inhibitory components in both ML and GL. Blocking GABA receptors abolished P1 in both ML and GL. Our results indicate that the facial stimulation evoked a simultaneous GABAergic inhibition in both ML and GL via mossy fiber-GC-parallel fiber pathway.

The cerebellar cortex is

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31460261, 31660272 and 31260245 and the international S & T cooperation program of China (2016YFE0128600).

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These authors contributed equally to this work.

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