Dynamic properties of sensory stimulation evoked responses in mouse cerebellar granule cell layer and molecular layer

Bing, Yan-Hua; Zhang, Guangjian; Sun, Lei; Chu, Chun-Ping; Qiu, De-Lai

doi:10.1016/j.neulet.2014.11.037

Cited by 16 publications

(16 citation statements)

References 22 publications

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“…In the present study, MLI–PC GABAergic transmission LTD was induced by 1 Hz, but not 2 Hz or 4 Hz, sensory stimulation in vivo in mice, suggesting that sensory stimulation-evoked LTD of MLI–PC synaptic transmission is stimulation-frequency-dependent. The cerebellar MLI network acts as a low-pass filter during the processing of high-frequency sensory information, and plays a critical role in the sensory-related outputs of PCs in the cerebellar cortex (Chu et al, 2012 ; Bing et al, 2015a ). However, cerebellar PCs generate sensory-related output that is limited to low-frequency sensory stimulation, and is independent of GABA A receptor-mediated inhibition (Bing et al, 2015b ).…”

Section: Discussionmentioning

confidence: 99%

Facial stimulation induces long-term depression at cerebellar molecular layer interneuronâ€“Purkinje cell synapses in vivo in mice

Bing

Chu

et al. 2015

Front. Cell. Neurosci.

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Cerebellar long-term synaptic plasticity has been proposed to provide a cellular mechanism for motor learning. Numerous studies have demonstrated the induction and mechanisms of synaptic plasticity at parallel fiber–Purkinje cell (PF–PC), parallel fiber–molecular layer interneurons (PF–MLI) and mossy fiber–granule cell (MF–GC) synapses, but no study has investigated sensory stimulation-evoked synaptic plasticity at MLI–PC synapses in the cerebellar cortex of living animals. We studied the expression and mechanism of MLI–PC GABAergic synaptic plasticity induced by a train of facial stimulation in urethane-anesthetized mice by cell-attached recordings and pharmacological methods. We found that 1 Hz, but not a 2 Hz or 4 Hz, facial stimulation induced a long-term depression (LTD) of GABAergic transmission at MLI–PC synapses, which was accompanied with a decrease in the stimulation-evoked pause of spike firing in PCs, but did not induce a significant change in the properties of the sensory-evoked spike events of MLIs. The MLI–PC GABAergic LTD could be prevented by blocking cannabinoid type 1 (CB1) receptors, and could be pharmacologically induced by a CB1 receptor agonist. Additionally, 1 Hz facial stimulation delivered in the presence of a metabotropic glutamate receptor 1 (mGluR1) antagonist, JNJ16259685, still induced the MLI–PC GABAergic LTD, whereas blocking N-methyl-D-aspartate (NMDA) receptors during 1 Hz facial stimulation abolished the expression of MLI–PC GABAergic LTD. These results indicate that sensory stimulation can induce an endocannabinoid (eCB)-dependent LTD of GABAergic transmission at MLI–PC synapses via activation of NMDA receptors in cerebellar cortical Crus II in vivo in mice. Our results suggest that the sensory stimulation-evoked MLI–PC GABAergic synaptic plasticity may play a critical role in motor learning in animals.

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Section: Discussionmentioning

confidence: 99%

Facial stimulation induces long-term depression at cerebellar molecular layer interneuronâ€“Purkinje cell synapses in vivo in mice

Bing

Chu

et al. 2015

Front. Cell. Neurosci.

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“…To observe facial stimulation-evoked MF–GC synaptic transmission, we recorded the facial stimulation-evoked field potential response in the cerebellar GL in the presence of the GABA A receptor antagonist picrotoxin (100 μM), which blocks the inhibitory components of Golgi cells. Blockade of GABA A receptor activity and air-puff stimulation of the ipsilateral whisker pad (60 ms; 50–60 psi) evoked negative components N1 and N2 in the GL ( Figure 1A ), which were identified as components of facial stimulation-evoked MF–GC synaptic transmission ( Bing et al, 2015a , b ; Ma et al, 2019 ). To determine the effects of chronic ethanol exposure on facial stimulation-evoked MF–GC synaptic transmission, we compared the properties of the facial stimulation-evoked field potential response in the GL between chronic ethanol-exposed and non-ethanol-exposed (control) mice.…”

Section: Resultsmentioning

confidence: 99%

“…The spike output of GCs could reflect the sensory information coding principal during the low-intensity rate-coded MF activation ( Arenz et al, 2008 ). GCs exhibit high-frequency and high-fidelity properties in response to sensory stimulation, which ensures the transmission of accurate sensory information to PCs ( van Beugen et al, 2013 ; Bing et al, 2015b ). In addition, GCs activate Golgi cells via parallel fibers ( Cesana et al, 2013 ), which inhibit GCs via Golgi axon branches ( Mapelli et al, 2009 ).…”

Section: Introductionmentioning

confidence: 99%

Chronic Ethanol Exposure Enhances Facial Stimulation-Evoked Mossy Fiber–Granule Cell Synaptic Transmission via GluN2A Receptors in the Mouse Cerebellar Cortex

GuangHui

et al. 2021

Front. Syst. Neurosci.

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Sensory information is transferred to the cerebellar cortex via the mossy fiber–granule cell (MF–GC) pathway, which participates in motor coordination and motor learning. We previously reported that chronic ethanol exposure from adolescence facilitated the sensory-evoked molecular layer interneuron–Purkinje cell synaptic transmission in adult mice in vivo. Herein, we investigated the effect of chronic ethanol exposure from adolescence on facial stimulation-evoked MF–GC synaptic transmission in the adult mouse cerebellar cortex using electrophysiological recording techniques and pharmacological methods. Chronic ethanol exposure from adolescence induced an enhancement of facial stimulation-evoked MF–GC synaptic transmission in the cerebellar cortex of adult mice. The application of an N-methyl-D-aspartate receptor (NMDAR) antagonist, D-APV (250 μM), induced stronger depression of facial stimulation-evoked MF–GC synaptic transmission in chronic ethanol-exposed mice compared with that in control mice. Chronic ethanol exposure-induced facilitation of facial stimulation evoked by MF–GC synaptic transmission was abolished by a selective GluN2A antagonist, PEAQX (10 μM), but was unaffected by the application of a selective GluN2B antagonist, TCN-237 (10 μM), or a type 1 metabotropic glutamate receptor blocker, JNJ16259685 (10 μM). These results indicate that chronic ethanol exposure from adolescence enhances facial stimulation-evoked MF–GC synaptic transmission via GluN2A, which suggests that chronic ethanol exposure from adolescence impairs the high-fidelity transmission capability of sensory information in the cerebellar cortex by enhancing the NMDAR-mediated components of MF–GC synaptic transmission in adult mice in vivo.

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“…Air-puff (60 ms, 50-60 psi) of the ipsilateral whisker pad evoked a paired-negative components N1, N2, accompanied with a positive component P1 in the GL of cerebellar cortical folium Crus II (Figure 1A). According to our previous studies (Wu et al, 2014;Bing et al, 2015;Ma et al, 2019), N1 and N2 were identified as MF-GC synaptic transmission which evoked by the stimulation-on (N1) and stimulation-off (N2), respectively. P1 was identified as GABAergic inhibitory components which could be abolished by GABA A receptor blocker.…”

Section: Methodsmentioning

confidence: 99%

Effect of Noradrenaline on the Facial Stimulation-Evoked Mossy Fiber-Granule Cell Synaptic Transmission in Mouse Cerebellar Cortex

Jin

Zhang

et al. 2021

Front. Neurosci.

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Noradrenaline is an important neuromodulator in the cerebellum. We previously found that noradrenaline depressed cerebellar Purkinje cell activity and climbing fiber–Purkinje cell synaptic transmission in vivo in mice. In this study, we investigated the effect of noradrenaline on the facial stimulation-evoked cerebellar cortical mossy fiber–granule cell synaptic transmission in urethane-anesthetized mice. In the presence of a γ-aminobutyrateA (GABAA) receptor antagonist, air-puff stimulation of the ipsilateral whisker pad evoked mossy fiber–granule cell synaptic transmission in the cerebellar granular layer, which expressed stimulus onset response, N1 and stimulus offset response, N2. Cerebellar surface perfusion of 25 μM noradrenaline induced decreases in the amplitude and area under the curve of N1 and N2, accompanied by an increase in the N2/N1 ratio. In the presence of a GABAA receptor blocker, noradrenaline induced a concentration-dependent decrease in the amplitude of N1, with a half-maximal inhibitory concentration of 25.45 μM. The noradrenaline-induced depression of the facial stimulation-evoked mossy fiber–granule cell synaptic transmission was reversed by additional application of an alpha-adrenergic receptor antagonist or an alpha-2 adrenergic receptor antagonist, but not by a beta-adrenergic receptor antagonist or an alpha-1 adrenergic receptor antagonist. Moreover, application of an alpha-2 adrenergic receptor agonist, UK14304, significantly decreased the synaptic response and prevented the noradrenaline-induced depression. Our results indicate that noradrenaline depresses facial stimulation-evoked mossy fiber–granule cell synaptic transmission via the alpha-2 adrenergic receptor in vivo in mice, suggesting that noradrenaline regulates sensory information integration and synaptic transmission in the cerebellar cortical granular layer.

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Dynamic properties of sensory stimulation evoked responses in mouse cerebellar granule cell layer and molecular layer

Cited by 16 publications

References 22 publications

Facial stimulation induces long-term depression at cerebellar molecular layer interneuronâ€“Purkinje cell synapses in vivo in mice

Facial stimulation induces long-term depression at cerebellar molecular layer interneuronâ€“Purkinje cell synapses in vivo in mice

Chronic Ethanol Exposure Enhances Facial Stimulation-Evoked Mossy Fiber–Granule Cell Synaptic Transmission via GluN2A Receptors in the Mouse Cerebellar Cortex

Effect of Noradrenaline on the Facial Stimulation-Evoked Mossy Fiber-Granule Cell Synaptic Transmission in Mouse Cerebellar Cortex

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