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Activation of group I metabotropic glutamate receptors regulates the excitability of rat retinal ganglion cells by suppressing Kir and I h

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Abstract

Group I metabotropic glutamate receptor (mGluR I) activation exerts a slow postsynaptic excitatory effect in the CNS. Here, the issues of whether and how this receptor is involved in regulating retinal ganglion cell (RGC) excitability were investigated in retinal slices using patch-clamp techniques. Under physiological conditions, RGCs displayed spontaneous firing. Extracellular application of LY367385 (10 µM)/MPEP (10 µM), selective mGluR1 and mGluR5 antagonists, respectively, significantly reduced the firing frequency, suggesting that glutamate endogenously released from bipolar cells constantly modulates RGC firing. DHPG (10 µM), an mGluR I agonist, significantly increased the firing and caused depolarization of the cells, which were reversed by LY367385, but not by MPEP, suggesting the involvement of the mGluR1 subtype. Intracellular Ca2+-dependent PI-PLC/PKC and calcium/calmodulin-dependent protein kinase II (CaMKII) signaling pathways mediated the DHPG-induced effects. In the presence of cocktail synaptic blockers (CNQX, D-AP5, bicuculline, and strychnine), which terminated the spontaneous firing in both ON and OFF RGCs, DHPG still induced depolarization and triggered the cells to fire. The DHPG-induced depolarization could not be blocked by TTX. In contrast, Ba2+, an inwardly rectifying potassium channel (Kir) blocker, and Cs+ and ZD7288, hyperpolarization-activated cation channel (I h) blockers, mimicked the effect of DHPG. Furthermore, in the presence of Ba2+/ZD7288, DHPG did not show further effects. Moreover, Kir and I h currents could be recorded in RGCs, and extracellular application of DHPG indeed suppressed these currents. Our results suggest that activation of mGluR I regulates the excitability of rat RGCs by inhibiting Kir and I h.

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Abbreviations

ACs:

Amacrine cells

ACSF:

Artificial cerebral spinal fluid

BCs:

Bipolar cells

Bis IV:

Bisindolylmaleimide IV

CaMKII:

Calcium/calmodulin-dependent protein kinase II

CNQX:

6-Cyano-7-nitroquinoxaline-2,3-dione

CNS:

Central nervous system

CV:

Coefficient of variation

D-APV:

d-(-)-2-amino-5-phosphonopentanoic acid

DHPG:

(S)-3,5-Dihydroxyphenylglycine

DMSO:

Dimethyl sulfoxide

EGTA:

Ethylene glycol-bis (β-aminoethyl ether) N,N,N′,N′-tetraacetic acid

EPSCs:

Excitatory postsynaptic currents

GCL:

Ganglion cell layer

HEPES:

4-(2-Hydroxyethyl)piperazine-1-ethanesulfonic acid

I h :

Hyperpolarization-activated cation channels

INL:

Inner nuclear layer

IPL:

Inner plexiform layer

ISI:

Interspike interval

Kir:

Inwardly rectifying potassium channels

OPL:

Outer plexiform layer

ONL:

Outer nuclear layer

PB:

Phosphate buffer

PBS:

Phosphate buffer saline

PFA:

Paraformaldehyde

PKC:

Protein kinase C

PLC:

Phospholipase C

mGluRs:

Metabotropic glutamate receptors

RGCs:

Retinal ganglion cells

TTX:

Tetrodotoxin

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Acknowledgments

This work was supported by Grants from the National Program of Basic Research of China (2013CB835100), the National Natural Science Foundation of China (31271173; 31470054; 81430007), the Key Research Program of Science and Technology Commissions of Shanghai Municipality (13DJ1400302), and the Natural Science Foundation of Shanghai, China (14ZR1402200).

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    1. Institutes of Brain Science, Fudan University, 138 Yixueyuan Rd, Shanghai, 200032, China

      Qian Li, Peng Cui, Yanying Miao, Feng Gao, Xue-Yan Li, Wen-Jing Qian, Shu-Xia Jiang, Na Wu, Xing-Huai Sun & Zhongfeng Wang

    2. Eye & ENT Hospital, Fudan University, Shanghai, 200031, China

      Feng Gao, Na Wu, Xing-Huai Sun & Zhongfeng Wang

    3. Institute of Neurobiology, Fudan University, Shanghai, 200032, China

      Qian Li, Peng Cui, Yanying Miao, Xue-Yan Li, Wen-Jing Qian, Shu-Xia Jiang & Zhongfeng Wang

    4. State Key Laboratory of Medical Neurobiology, Fudan University, Shanghai, 200032, China

      Qian Li, Peng Cui, Yanying Miao, Feng Gao, Xue-Yan Li, Wen-Jing Qian, Shu-Xia Jiang, Na Wu, Xing-Huai Sun & Zhongfeng Wang

    5. Shanghai Key Laboratory of Visual Impairment and Restoration, Fudan University, Shanghai, 200031, China

      Feng Gao, Na Wu, Xing-Huai Sun & Zhongfeng Wang

    6. Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, 200032, China

      Qian Li, Peng Cui, Yanying Miao, Feng Gao, Xue-Yan Li, Wen-Jing Qian, Shu-Xia Jiang, Na Wu, Xing-Huai Sun & Zhongfeng Wang

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    Q. Li and P. Cui contributed equally to this work.

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    Li, Q., Cui, P., Miao, Y. et al. Activation of group I metabotropic glutamate receptors regulates the excitability of rat retinal ganglion cells by suppressing Kir and I h . Brain Struct Funct 222, 813–830 (2017). https://doi.org/10.1007/s00429-016-1248-3

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