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Chrna2-Martinotti Cells Synchronize Layer 5 Type a Pyramidal Cells Via Rebound Excitation

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Chrna2-Martinotti Cells Synchronize Layer 5 Type a Pyramidal Cells Via Rebound Excitation RESEARCH ARTICLE Chrna2-Martinotti Cells Synchronize Layer 5 Type A Pyramidal Cells via Rebound Excitation Markus M. Hilscher1,2*, Richardson N. Leão1,2, Steven J. Edwards1, Katarina E. Leão2☯, Klas Kullander1☯* 1 Unit of Developmental Genetics, Department of Neuroscience, Uppsala University, Uppsala, Sweden, 2 Brain Institute, Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil ☯ These authors contributed equally to this work. * [email protected] (MMH); [email protected] (KK) a1111111111 a1111111111 a1111111111 a1111111111 Abstract a1111111111 Martinotti cells are the most prominent distal dendrite±targeting interneurons in the cortex, but their role in controlling pyramidal cell (PC) activity is largely unknown. Here, we show that the nicotinic acetylcholine receptor α2 subunit (Chrna2) specifically marks layer 5 (L5) Martinotti cells projecting to layer 1. Furthermore, we confirm that Chrna2-expressing Marti- OPEN ACCESS notti cells selectively target L5 thick-tufted type A PCs but not thin-tufted type B PCs. Using Citation: Hilscher MM, Leão RN, Edwards SJ, Leão optogenetic activation and inhibition, we demonstrate how Chrna2-Martinotti cells robustly KE, Kullander K (2017) Chrna2-Martinotti Cells reset and synchronize type A PCs via slow rhythmic burst activity and rebound excitation. Synchronize Layer 5 Type A Pyramidal Cells via Rebound Excitation. PLoS Biol 15(2): e2001392. Moreover, using optical feedback inhibition, in which PC spikes controlled the firing of sur- doi:10.1371/journal.pbio.2001392 rounding Chrna2-Martinotti cells, we found that neighboring PC spike trains became syn- Academic Editor: Alberto Bacci, ICM - Institut du chronized by Martinotti cell inhibition. Together, our results show that L5 Martinotti cells Cerveau et de la Moelle eÂpinière, France participate in defined cortical circuits and can synchronize PCs in a frequency-dependent Received: October 21, 2016 manner. These findings suggest that Martinotti cells are pivotal for coordinated PC activity, which is involved in cortical information processing and cognitive control. Accepted: January 5, 2017 Published: February 9, 2017 Copyright: © 2017 Hilscher et al. This is an open access article distributed under the terms of the Author Summary Creative Commons Attribution License, which permits unrestricted use, distribution, and Cognitive functions and information processing are linked to the coordination of neuro- reproduction in any medium, provided the original nal events and activities. This coordination is achieved through the synchronization of author and source are credited. neuronal signals within subnetworks. Local networks contain different types of nerve Data Availability Statement: All relevant data are cells, each of them playing distinct roles in the synchronization mechanism. To under- within the paper and its Supporting Information stand how synchronization is initiated and maintained, we have identified one of the files. key players using genetic strategies; we have identified a subtype of nicotine receptors Funding: Swedish Foundation for International uniquely expressed in cortical Martinotti cells. Because of their architecture and connec- Cooperation in Research and Higher Education tion properties, Martinotti cells are able to synchronize ongoing activity of unconnected (STINT) www.stint.se. Received by RNL and KK. pyramidal cells (PCs). We show that this mechanism only applies to one subtype of PCs, The funder had no role in study design, data collection and analysis, decision to publish, or thereby demonstrating that Martinotti cell inhibition is not spread randomly. By testing preparation of the manuscript. American Tinnitus optimal firing patterns of Martinotti cells, we are able to coordinate the firing of this spe- Association www.ata.org. Received by MMH, RNL, cific PC subtype over longer periods of time, showing how one unique interneuron is con- and KEL. The funder had no role in study design, tributing to information processing. data collection and analysis, decision to publish, or PLOS Biology | DOI:10.1371/journal.pbio.2001392 February 9, 2017 1 / 26 Synchronization by Chrna2-Martinotti Cells preparation of the manuscript. Brazilian National Introduction Council of Technological and Scientific Development (CNPq) www.cnpq.br. Received by Martinotti cells, ubiquitous to the cortex [1], are the most prominent cross-laminar interneu- MMH, RNL, and KEL. The funder had no role in ron subtype forming synapses in layer 1 onto the distal dendrites of cortical pyramidal cells study design, data collection and analysis, decision (PCs) [1±3]. Despite this close structural relationship, the role of Martinotti cell inhibition is to publish, or preparation of the manuscript. not clear. Studies identifying Martinotti cells by various markers have found different mor- Brazilian Federal Agency for Support and phologies and microcircuit connectivity depending on the cortical layer in which their cell Evaluation of Graduate Education (CAPES) www. capes.gov.br. Received by MMH, RNL, and KEL. bodies reside [2]. In general, the division of neocortical interneurons into either parvalbumin-, The funder had no role in study design, data somatostatin (SOM)-, or 5HT3aR-expressing cells [4±6] has been helpful for dissecting neural collection and analysis, decision to publish, or functionality; yet, these groups can be further subdivided and show partial overlap between preparation of the manuscript. Swedish Research interneuron markers. Martinotti cells are a subclass of SOM+ cells [7,2,4], and several combi- Council www.vr.se. Received by KK. The funder nations of transgenic lines have been created to try to genetically and morphologically isolate had no role in study design, data collection and Martinotti cells [8±10]. For example, the SOM-cyclization recombinase (Cre) mouse line analysis, decision to publish, or preparation of the manuscript. Swedish Brain Foundation www. marks layer 1±projecting Martinotti cells with cell bodies in both layer 5 (L5) and layer 2/3 hjarnfonden.se. Received by KK. The funder had no (infragranular and supragranular layers) but also labels non-Martinotti cells in layer 4 [10]. role in study design, data collection and analysis, Although electrophysiologically, SOM+ Martinotti cells are often referred to as low-threshold decision to publish, or preparation of the spiking (LTS) neurons [3] or slow-inhibitory interneurons [11], early studies have shown up manuscript. to four different firing patterns for Martinotti cells [2,9]. Competing Interests: The authors have declared Functionally, cortical SOM+ interneurons have been suggested to provide a ªblanket of that no competing interests exist. inhibitionº [12], a dense and nonspecific spread of inhibition on nearby PCs. Whether Marti- Abbreviations: ADP, afterdepolarization; AHP, notti cells are capable of generating such indiscriminate inhibition when firing simultaneously afterhyperpolarization; AP, action potential; ChR2, in large groups has not been tested. Martinotti cells that reside in the main cortical output L5 Channelrhodopsin-2; Chrna2, nicotinic provide frequency-dependent disynaptic inhibition (FDDI) on neighboring PCs [13,14], an acetylcholine receptor 2 subunit; Cre, cyclization α inhibitory mechanism that synchronizes two or more PCs by one or a few Martinotti cells recombinase; EPSC, excitatory postsynaptic current; EPSP, excitatory postsynaptic potential; [15]. Synchronized activities in the cortex have been reported in vivo [16] as well as in vitro, FDDI, frequency-dependent disynaptic inhibition; where slow oscillations appear to be initiated in L5 [17]. Moreover, computational studies sug- GAD1, Glutamate decarboxylase 1; GIN cell, a type gest that Martinotti cell activity can synchronize L5 PC spiking through distal inhibition [18]; of somatostatin-expressing interneuron defined by however, this has not been tested experimentally. It is intriguing that distal dendrite±targeting its green fluorescent protein expression in a interneurons, generating attenuated inhibitory currents, can affect PC spike time output. transgenic mouse; HaloR, Halorhodopsin; IPSP, Here, we genetically targeted the L5 Martinotti cell population using a nicotinic acetylcholine inhibitory postsynaptic potential; L5, layer 5; LTS, low-threshold spiking; MCsα2, L5-specific Chrna2- receptor α2 subunit (Chrna2)-Cre mouse line to investigate how Martinotti cell inhibition can Martinotti cells; nAChR, nicotinic acetylcholine synchronize L5 PC firing. Our results show that Chrna2-Cre±labeled L5 Martinotti cells were receptor; OLM, oriens-lacunosum moleculare; PC, preferentially and reciprocally connected with thick-tufted PCs. Furthermore, we found that pyramidal cell; RT-PCR, reverse transcription PCR; short burst firing of L5 Martinotti cells was able to reset L5 PC spiking and that controlling SEM, standard error of the mean; SOM, Martinotti cell activity to rapid bursts repeated in a slow rhythm was the most efficient inhibi- somatostatin; VIP, vasoactive intestinal peptide. tion to synchronize unconnected PCs. Finally, we show that L5 PC microcircuits could syn- chronize their own action potentials (APs) when coupled by L5 Martinotti cells and that inhibition was crucial for PC synchronization over prolonged periods. Results L5 Martinotti Cells Express the Nicotinic Acetylcholine Receptor Subunit Alpha 2 To test whether Chrna2 can be used as a marker of Martinotti cells, we crossed Chrna2-Cre mice with a tdTomato reporter
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