Morphology and function of three VIP-expressing amacrine cell types in the mouse retina

Author:

Akrouh Alejandro12,Kerschensteiner Daniel1345

Affiliation:

1. Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, Missouri;

2. Graduate Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri;

3. Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri;

4. Department of Biomedical Engineering, Washington University School of Medicine, St. Louis, Missouri; and

5. Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, Missouri

Abstract

Amacrine cells (ACs) are the most diverse class of neurons in the retina. The variety of signals provided by ACs allows the retina to encode a wide range of visual features. Of the 30–50 AC types in mammalian species, few have been studied in detail. Here, we combine genetic and viral strategies to identify and to characterize morphologically three vasoactive intestinal polypeptide-expressing GABAergic AC types (VIP1-, VIP2-, and VIP3-ACs) in mice. Somata of VIP1- and VIP2-ACs reside in the inner nuclear layer and somata of VIP3-ACs in the ganglion cell layer, and they show asymmetric distributions along the dorsoventral axis of the retina. Neurite arbors of VIP-ACs differ in size (VIP1-ACs ≈ VIP3-ACs > VIP2-ACs) and stratify in distinct sublaminae of the inner plexiform layer. To analyze light responses and underlying synaptic inputs, we target VIP-ACs under 2-photon guidance for patch-clamp recordings. VIP1-ACs depolarize strongly to light increments (ON) over a wide range of stimulus sizes but show size-selective responses to light decrements (OFF), depolarizing to small and hyperpolarizing to large stimuli. The switch in polarity of OFF responses is caused by pre- and postsynaptic surround inhibition. VIP2- and VIP3-ACs both show small depolarizations to ON stimuli and large hyperpolarizations to OFF stimuli but differ in their spatial response profiles. Depolarizations are caused by ON excitation outweighing ON inhibition, whereas hyperpolarizations result from pre- and postsynaptic OFF-ON crossover inhibition. VIP1-, VIP2-, and VIP3-ACs thus differ in response polarity and spatial tuning and contribute to the diversity of inhibitory and neuromodulatory signals in the retina.

Funder

Office of Extramural Research, National Institutes of Health (OER)

National Science Foundation (NSF)

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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