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Morphology and Function of Three VIP-Expressing Amacrine Cell Types in the Mouse Retina

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Morphology and Function of Three VIP-Expressing Amacrine Cell Types in the Mouse Retina J Neurophysiol 114: 2431–2438, 2015. First published August 26, 2015; doi:10.1152/jn.00526.2015. Morphology and function of three VIP-expressing amacrine cell types in the mouse retina Alejandro Akrouh1,2 and Daniel Kerschensteiner1,3,4,5 1Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, Missouri; 2Graduate Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri; 3Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri; 4Department of Biomedical Engineering, Washington University School of Medicine, St. Louis, Missouri; and 5Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, Missouri Submitted 1 June 2015; accepted in final form 21 August 2015 Akrouh A, Kerschensteiner D. Morphology and function of Thirteen bipolar cell types carry different components of three VIP-expressing amacrine cell types in the mouse retina. J photoreceptor signals from the outer to the inner retina (i.e., Neurophysiol 114: 2431–2438, 2015. First published August 26, parallel pathways), where their axons target specific sublami- 2015; doi:10.1152/jn.00526.2015.—Amacrine cells (ACs) are the nae of the inner plexiform layer (IPL; Euler et al. 2014). Some most diverse class of neurons in the retina. The variety of signals AC types extend neurites in multiple sublaminae of the IPL and 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 likely mediate interactions between pathways (Menger et al. been studied in detail. Here, we combine genetic and viral strate- 1998; Werblin 2010), whereas others target a single sublamina gies to identify and to characterize morphologically three vasoac- and likely mediate interactions within a pathway (Briggman et tive intestinal polypeptide-expressing GABAergic AC types al. 2011; Lin and Masland 2006). In addition, AC types differ (VIP1-, VIP2-, and VIP3-ACs) in mice. Somata of VIP1- and greatly in the size of lateral territories their neurites cover and, VIP2-ACs reside in the inner nuclear layer and somata of VIP3- as a result, the areas of visual space from which they receive ACs in the ganglion cell layer, and they show asymmetric distri- input (Masland 2012). Gene expression profiles match the butions along the dorsoventral axis of the retina. Neurite arbors of morphological diversity of ACs (Cherry et al. 2009; Kay et al. Ϸ Ͼ VIP-ACs differ in size (VIP1-ACs VIP3-ACs VIP2-ACs) and 2011; Siegert et al. 2012) and support a range of AC output stratify in distinct sublaminae of the inner plexiform layer. To signals. In addition to GABA or glycine, many AC types analyze light responses and underlying synaptic inputs, we target release neuromodulators including bioactive peptides (Bagnoli VIP-ACs under 2-photon guidance for patch-clamp recordings. VIP1-ACs depolarize strongly to light increments (ON) over a et al. 2003; Gustincich et al. 1997; Vaney 2004). Few AC types wide range of stimulus sizes but show size-selective responses to have been functionally characterized, due in part to the limited light decrements (OFF), depolarizing to small and hyperpolarizing accessibility of their somata in the middle of the retina and a to large stimuli. The switch in polarity of OFF responses is caused paucity of tools for cell-type-specific targeting. The comple- by pre- and postsynaptic surround inhibition. VIP2- and VIP3-ACs ment of inhibitory and neuromodulatory signals that shape both show small depolarizations to ON stimuli and large hyperpo- visual processing in the retina, therefore, remains mostly un- larizations to OFF stimuli but differ in their spatial response explored. profiles. Depolarizations are caused by ON excitation outweighing Here, we combine genetic and viral strategies to identify ON inhibition, whereas hyperpolarizations result from pre- and postsyn- and characterize three AC types expressing vasoactive in- aptic OFF-ON crossover inhibition. VIP1-, VIP2-, and VIP3-ACs testinal polypeptide (VIP-ACs) in the mouse retina. VIP- thus differ in response polarity and spatial tuning and contribute to the diversity of inhibitory and neuromodulatory signals in the ACs have been identified in several species, including hu- retina. mans (Tornqvist and Ehinger 1988), monkeys (Lammerd- ing-Koppel et al. 1991), rabbits (Casini and Brecha 1991, amacrine cell; receptive field; retina; VIP 1992; Sagar 1987), guinea pigs (Lee et al. 2002), and rats (Terubayashi et al. 1983). Single-cell anatomy has only IN MANY PARTS OF THE NERVOUS SYSTEM, the diversity of local been examined in a few studies and appears to differ circuit neurons, or interneurons, exceeds that of projection between species as does the number of VIP-AC types neurons (Markram et al. 2004; Somogyi and Klausberger 2005; (Lammerding-Koppel et al. 1991; Lee et al. 2002). Func- Taniguchi et al. 2011). The diversity of interneurons may be tional responses of VIP-ACs have not yet been reported. greatest in the retina, where 30–50 types of amacrine cells Here, we analyze the morphology of VIP-ACs, adding two (ACs) mediate interactions among bipolar cells, amacrine cells, types (VIP2- and VIP3-ACs) to the recently described and ganglion cells, the projection neurons that transmit visual VIP1-ACs (Zhu et al. 2014) in mice. We then target all three information to the brain (Helmstaedter et al. 2013; MacNeil VIP-AC types for patch-clamp recordings in retinal flat and Masland 1998; Masland 2012). mount preparation and find that, in accordance with their morphological diversity, they receive distinct combinations Address for reprint requests and other correspondence: D. Kerschensteiner, of excitatory and inhibitory input from ON and OFF path- Dept. of Ophthalmology and Visual Sciences, Washington Univ. School of ways over different areas of visual space. As a result, Medicine, St. Louis, MO 63110 (e-mail: [email protected]). VIP-AC types differ in response polarity and spatial re- www.jn.org 0022-3077/15 Copyright © 2015 the American Physiological Society 2431 2432 CHARACTERIZATION OF VIP-ACs sponse profiles contributing to the variety of signals in the MgCl2, 10 Na-HEPES, 11 EGTA, 10 TEA-Cl, and 2 Qx314 (pH inner retina. adjusted to 7.2 with CsOH). Patch pipettes had resistances of 4–7 M⍀ (borosilicate glass). All reported voltages were corrected for liquid junction potentials (voltage-clamp: Ϫ14 mV, current-clamp: Ϫ12.6 MATERIALS AND METHODS mV). Signals were amplified with a MultiClamp 700B amplifier Mice. All experiments were performed in young adult (postnatal (Molecular Devices), filtered at 3 kHz (8-pole Bessel low-pass), and days 25-35) VIP-ires-Cre (Taniguchi et al. 2011) mice crossed to a sampled at 10 kHz (Digidata 1440A; Molecular Devices). Excitatory fluorescent reporter strain (Ai9, tdTomato; Madisen et al. 2010) or and inhibitory postsynaptic currents were isolated by clamping the Ϫ injected with adeno-associated virus (AAV) vectors. Procedures were voltage of the recorded cell at the reversal potential for Cl (Ϫ60 mV) approved by the Animal Studies Committee of Washington University and cations (0 mV), respectively. In VIP1-ACs, gap junctions likely School of Medicine and performed in compliance with the National contribute to currents measured in voltage-clamp (Park et al. 2015). Institutes of Health Guide for the Care and Use of Laboratory Only cells in which current amplitudes to full-field contrast steps Animals. (50%) at the beginning and end of the recording varied by Ͻ10% were AAV. Two Brainbow AAV vectors (AAV9-hEF1a-lox-TagBFP- used for analysis. In current-clamp recordings, no bias current was lox-eYFP-lox-WPRE-hGH-InvBYF and AAV9-hEF1a-lox-mCherry- injected. The resting membrane potential of the three VIP-AC types lox-mTFP1-lox-WPRE-hGH-InvCheTF; Cai et al. 2013) were in- under these conditions was: VIP1-ACs, Ϫ50.5 Ϯ 2.2 mV, n ϭ 10; jected (1:1, 250–500 nl) into the vitreous of newborn VIP-ires-Cre VIP2-ACs, Ϫ49.2 Ϯ 3 mV, n ϭ 9; and VIP3-ACs, Ϫ41.7 Ϯ 3 mV, mice as described before (Soto et al. 2013), and retinas were examined n ϭ 5. 3–4 wk after the injection. Fluorescent somata in the INL and GCL of VIP-ires-Cre Ai9 Tissue preparation. Mice were euthanized, their eyes removed, mice were targeted under two-photon guidance (excitation wave- and retinas isolated as described previously (Akrouh and Ker- length: 900 nm). Correct targeting was confirmed by monitoring schensteiner 2013). For patch-clamp recordings, mice were dark- diffusion of a fluorescent dye (Alexa 488, 0.1 mM) from the adapted Ͼ2 h, and all subsequent procedures were performed recording electrode into the soma during break in. VIP1-, VIP2-, under infrared illumination (Ͼ900 nm). For imaging, retinal flat and VIP3-ACs were distinguished by the position of their somata mounts were fixed for 30 min with 4% paraformaldehyde in mouse (VIP1- and VIP2-ACs in INL and VIP3-ACs in GCL) and the artificial cerebrospinal fluid containing (in mM): 119 NaCl, 2.5 distinct arborization patterns and sizes of their neurites imaged at KCl, 1 NaH2PO4, 2.5 CaCl2, 1.3 MgCl2, 20 HEPES, and 11 the end of each recording. glucose (pH adjusted to 7.37 using NaOH). Visual stimuli and analysis. Stimuli were written in MATLAB (The Immunohistochemistry. Fixed retinal flat mounts and sections MathWorks) using Cogent Graphics extensions (John Romaya, Uni- were stained with primary antibodies against choline acetyltrans- versity College London) and were presented on an organic light- ferase (goat anti-ChAT; 1:1,000; Millipore) and VIP (rabbit anti- emitting display (refresh rate: 60 Hz; eMagin) focused onto photore- VIP; 1:1,000; Immunostar) visualized with secondary antibodies ceptors. The mean intensity of all stimuli was 2,500 rhodopsin coupled to Alexa 488 or Alexa 633 (1:1,000; Millipore).
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