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Neuronal Organization of Olfactory Bulb Circuits

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Neuronal Organization of Olfactory Bulb Circuits REVIEW ARTICLE published: 03 September 2014 doi: 10.3389/fncir.2014.00098 Neuronal organization of olfactory bulb circuits Shin Nagayama 1*, Ryota Homma1 and Fumiaki Imamura 2 1 Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston, Houston, TX, USA 2 Department of Pharmacology, Pennsylvania State University College of Medicine, Hershey, PA, USA Edited by: Olfactory sensory neurons extend their axons solely to the olfactory bulb, which is Benjamin R. Arenkiel, Baylor College dedicated to odor information processing.The olfactory bulb is divided into multiple layers, of Medicine, USA with different types of neurons found in each of the layers. Therefore, neurons in the Reviewed by: olfactory bulb have conventionally been categorized based on the layers in which their cell Kazushige Touhara, University of Tokyo, Japan bodies are found; namely, juxtaglomerular cells in the glomerular layer, tufted cells in the Veronica Egger, external plexiform layer, mitral cells in the mitral cell layer, and granule cells in the granule Ludwig-Maximilians-Universität, cell layer. More recently, numerous studies have revealed the heterogeneous nature of each Germany Kathleen Quast, Baylor College of of these cell types, allowing them to be further divided into subclasses based on differences Medicine, USA in morphological, molecular, and electrophysiological properties. In addition, technical *Correspondence: developments and advances have resulted in an increasing number of studies regarding Shin Nagayama, Department of cell types other than the conventionally categorized ones described above, including short- Neurobiology and Anatomy, The axon cells and adult-generated interneurons. Thus, the expanding diversity of cells in the University of Texas Medical School at Houston, 6431 Fannin Street, olfactory bulb is now being acknowledged. However, our current understanding of olfactory MSB 7.046, Houston, TX, USA bulb neuronal circuits is mostly based on the conventional and simplest classification of e-mail: [email protected] cell types. Few studies have taken neuronal diversity into account for understanding the function of the neuronal circuits in this region of the brain. This oversight may contribute to the roadblocks in developing more precise and accurate models of olfactory neuronal networks. The purpose of this review is therefore to discuss the expanse of existing work on neuronal diversity in the olfactory bulb up to this point, so as to provide an overall picture of the olfactory bulb circuit. Keywords: structure of olfactory bulb, cell type, layer formation INTRODUCTION Nei et al., 2008; Adipietro et al., 2012). Because each olfactory Our environment is filled with odorant molecules, and our emo- sensory neuron expresses only a single odorant receptor, differ- tions, moods, and even behaviors can be controlled by olfactory ent odorants can activate distinct subsets of olfactory sensory stimuli. We are predisposed to discriminate between more than neurons. Information from activated neurons is first transmit- 1012 odors (Bushdid et al., 2014), in part due to the variety of ted to the olfactory bulb. Several reviews have summarized the odorant receptors that bind to different odorants with unique elaborate neuronal network that extends from the olfactory epithe- affinity profiles (Malnic et al., 1999). These odorant receptors are lium to the olfactory bulb (Wilson and Mainen, 2006; Zou et al., expressed by olfactory sensory neurons in the olfactory epithe- 2009; Sakano, 2010; Mori and Sakano, 2011; Murthy, 2011; lium. Since the first rat odorant receptor was cloned in 1991, Lodovichi and Belluscio, 2012). In the olfactory bulb, multi- approximately 400 and 1000 different functional odorant recep- ple types of neurons form sophisticated networks to process tors have been identified in the human and mouse genome, information before transmitting it further to the olfactory cor- respectively (Buck and Axel, 1991; Zhang and Firestein, 2002; tex. Currently, there is a pressing demand for understanding the numerous neuronal types and networks to elucidate the mech- anism(s) of olfactory information processing in the olfactory Abbreviations: Brain areas: AON, anterior olfactory nucleus; AONpE, anterior olfactory nucleus pars externa; SVZ, subventicular zone; Layers: ONL, olfactory bulb. nerve layer; GL, glomerular layer; EPL, external plexiform layer; s-EPL, superfi- Histologically, the olfactory bulb is divided into multiple lay- cial EPL; i-EPL, intermediate EPL; d-EPL, deep EPL; MCL, mitral cell layer; IPL, ers. Intensive Golgi analyses in the 1970s succeeded in visualizing internal plexiform layer; GCL, granule cell layer; Cells: JG cell, juxtaglomerular the morphology of neurons in each layer, and showed that the cell; PG cell, periglomerular cell; ET cell, external tufted cell; sSA cell, superficial short-axon cell; dSA cell, deep short-axon cell; SRIF-ir cell, somatostatinimmunore- distinct layers were composed of morphologically distinct cells active cell; Molecules: BrdU, 5-bromo-2-deoxyuridine; CaMKIV, CaM kinase IV; (Price and Powell, 1970a,b; Pinching and Powell, 1971a). There- CB, calbindin; CCK, cholecystokinin; CR, calretinin; CRH, corticotropin-releasing fore, the neurons in the olfactory bulb have conventionally been hormone; DHPG, (RS)-3,5-dihydroxyphenylglycine; GAD, glutamic acid decar- boxylase; GFP, green fluorescent protein; HCN, hyperpolarization-activated cyclic categorized based on the layers in which their cell bodies are found. nucleotide gated channel; HRP, horseradish peroxidase; Kv, voltage-gated potas- According to this categorization, juxtaglomerular (JG) cells, mitral sium channel; mGluRs, metabotropic glutamate receptors; nNOS, neuronal nitric cells, tufted cells, and granule cells were first defined. JG cells oxide synthase; PV, parvalbumin; TH, tyrosine hydroxylase; VGAT, vesicular GABA are now known to include three morphologically distinct cell transporter; VGLUT, vesicular glutamate transporter; VIP, vasoactive intestinal polypeptide. types, the periglomerular (PG) cells, external tufted (ET) cells, and Frontiers in Neural Circuits www.frontiersin.org September 2014 | Volume 8 | Article 98 | 1 Nagayama et al. Olfactory bulb neuronal types/subtypes superficial short-axon (sSA) cells. This categorization provides us Nevertheless, new neuronal types and connections are often with a basic model of the olfactory bulb network (Figure 1). not taken into account in building a model of the olfactory bulb However, we are far away from forming a comprehensive network. We are concerned with this trend of omission as it may model of the olfactory bulb network. An increasing number of hinder future progress in research. The major problem is that novel studies suggest that conventionally categorized neurons in the findings are scattered across many literary references, and recent brain comprise heterogeneous populations, and that the neuronal reviews have not effectively summarized the neuronal diversity types in the olfactory bulb are among the most diverse (Shipley in the olfactory bulb. Here, we gather the scattered results and and Ennis, 1996). For example, PG cells are molecularly hetero- summarize the discoveries regarding the new neuronal types and geneous (Kosaka et al., 1995; Kosaka and Kosaka, 2005, 2007a; connections in each layer. Since understanding the inputs and Panzanelli et al., 2007; Parrish-Aungst et al., 2007), and subgroups outputs of neurons is fundamental to building a network model, of mitral cells with different morphological and/or electrophysio- we focus mainly on somata locations, axon/dendrite extension logical properties have been identified (Padmanabhan and Urban, patterns, neurotransmitters, and/or the physiological properties of 2010; Angelo et al., 2012). Furthermore, granule cells can be sep- neurons. We believe that this review greatly adds to our knowledge arated into morphologically distinct subgroups (Mori et al., 1983; of the general model of the olfactory bulb network, and brings the Orona et al., 1983), and divergent properties between granule information about this brain region to another level. In this article, cells generated during developmental and adult stages are noted we focus on neurons rather than on glia and the rodent main (Lemasson et al., 2005). In addition, some olfactory bulb neurons olfactory bulb rather than accessory olfactory bulb. The authors have not been typically included in conventional categories due to apologize to those whose work was not included here due to space their relatively small numbers [e.g., short-axon cells in the External limitations. plexiform layer (EPL) and the granule cell layer (GCL)]. Nonethe- less, recent technological advances now make it possible to target GLOMERULAR LAYER and analyze even these miniscule cell populations. Moreover, new NEURONS IN THE GLOMERULAR LAYER AND THEIR MORPHOLOGY neuronal types and connections in the olfactory bulb continue to Neurons in the glomerular layer (GL) are morphologically be discovered (Merkle et al., 2014). heterogeneous and are of three identified types, PG cells, sSA cells, FIGURE 1 | Basic model of the olfactory bulb network. The illustrated send their axons to the olfactory cortex. The somata of mitral cells are located olfactory bulb network is based on the conventional categorization of in the mitral cell layer (MCL), while the tufted cells are scattered throughout participating neurons. The axons of olfactory sensory neurons make synapses the EPL.
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