Glutamatergic Monopolar Interneurons Provide a Novel Pathway of Excitation in the Mouse Retina

Luca Della Santina, Sidney P. Kuo, Takeshi Yoshimatsu, Haruhisa Okawa, Sachihiro C. Suzuki, Mrinalini Hoon, Kotaro Tsuboyama, Fred Rieke, Rachel O.L. Wong

Research output: Contribution to journalArticlepeer-review

27 Scopus citations

Abstract

Excitatory and inhibitory neurons in the CNS are distinguished by several features, including morphology, transmitter content, and synapse architecture [1]. Such distinctions are exemplified in the vertebrate retina. Retinal bipolar cells are polarized glutamatergic neurons receiving direct photoreceptor input, whereas amacrine cells are usually monopolar inhibitory interneurons with synapses almost exclusively in the inner retina [2]. Bipolar but not amacrine cell synapses have presynaptic ribbon-like structures at their transmitter release sites. We identified a monopolar interneuron in the mouse retina that resembles amacrine cells morphologically but is glutamatergic and, unexpectedly, makes ribbon synapses. These glutamatergic monopolar interneurons (GluMIs) do not receive direct photoreceptor input, and their light responses are strongly shaped by both ON and OFF pathway-derived inhibitory input. GluMIs contact and make almost as many synapses as type 2 OFF bipolar cells onto OFF-sustained A-type (AOFF-S) retinal ganglion cells (RGCs). However, GluMIs and type 2 OFF bipolar cells possess functionally distinct light-driven responses and may therefore mediate separate components of the excitatory synaptic input to AOFF-S RGCs. The identification of GluMIs thus unveils a novel cellular component of excitatory circuits in the vertebrate retina, underscoring the complexity in defining cell types even in this well-characterized region of the CNS.

Original languageEnglish (US)
Pages (from-to)2070-2077
Number of pages8
JournalCurrent Biology
Volume26
Issue number15
DOIs
StatePublished - Aug 8 2016

Bibliographical note

Funding Information:
All procedures were performed in accordance with University of Washington Institutional Animal Care and Use Committee-approved protocols. This work was supported by the National Institute of Health (EY017101 to R.O.L.W., EY11850 to F.R., and Center Core Grant for Vision Research EY01730) and Howard Hughes Medical Institute (F.R.). K.T. (Medical Scientist Training Program at the University of Tokyo) was supported by a Government Subsidy for Management Expenses travel award. We thank J.M. Fritschy for kindly providing GABA A antibodies and R. Enz and H. Wässle for kindly providing the GABA C antibody.

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