Molecules and Cells Minireview Distinct Developmental Features of Olfactory Bulb Interneurons 1 1 1,2,3, Jae Yeon Kim , Jiyun Choe , and Cheil Moon * Department of Brain and Cognitive Sciences, Graduate School, Daegu Gyeongbuk Institute of Science and Technology, Daegu 42988, Korea, Convergence Research Advanced Centre for Olfaction, Daegu Gyeongbuk Institute of Science and Technology, Daegu 42988, Korea, Korea Brain Research Institute, Daegu 41062, Korea *Correspondence: firstname.lastname@example.org https://doi.org/10.14348/molcells.2020.0033 www.molcells.org The olfactory bulb (OB) has an extremely higher proportion these diverse neuronal functions, interneurons are developed of interneurons innervating excitatory neurons than other into morphologically, molecularly, and electrophysiologically brain regions, which is evolutionally conserved across species. diverse subtypes and are continuously generated from embry- Despite the abundance of OB interneurons, little is known onic to even adult stages (Bartolini et al., 2013; Batista-Brito about the diversification and physiological functions of and Fishell, 2009; Kepecs and Fishell, 2014). Malformation of OB interneurons compared to cortical interneurons. In this the interneurons during early development can lead to neu- review, an overview of the general developmental process rodevelopmental disorders, such as autism spectrum disorder of interneurons from the angles of the spatial and temporal (ASD) and Tourette’s syndrome (Ashwin et al., 2014; Marco specifications was presented. Then, the distinct features et al., 2011). Thus, defining neuronal properties and classify- shown exclusively in OB interneurons development and ing the myriad of diverse interneurons are essential for under- molecular machinery recently identified were discussed. standing complex brain physiologies (Maccaferri and Lacaille, Finally, we proposed an evolutionary meaning for the 2003), as well as neurodevelopmental disorders (Fang et al., diversity of OB interneurons. 2014). Mammalian OB express the most abundant and varied in- Keywords: development, diversity, interneuron, olfactory terneurons in the brain, but they have received little attention bulb, spatio-temporal specification compared to cortical interneurons. Approximately 90% of ASD patients having mental retardation have a high sensitivity to external auditory stimuli and some of patients are suffered from hallucinations of olfaction (Galle et al., 2013; Gomes et INTRODUCTION al., 2008; Tonacci et al., 2017). Furthermore, the abnormal Identification of the neuronal components in the brain pro- structural development of OB interneurons in the early stage vides important insight for understanding high-order and induces olfactory impairments (Kim et al., 2020; Yoshihara et complicated behaviors, including logical thinking, emotional al., 2014). These facts indicated that research on the devel- sensation, and interaction with external signals (Ramón y opment of interneurons in the OB is critical and fundamental. Cajal et al., 1988). Specifically, interneurons control neuro- In this review, we introduced the distinct characteristics of OB transmission by the intricate modulation of information pro- interneuron development by comparing them to the com- cessing (Bartolini et al., 2013; Paredes et al., 2016). To adapt mon developmental features of other interneurons. We also Received 30 January, 2020; revised 27 February, 2020; accepted 2 March, 2020; published online 17 March, 2020 eISSN: 0219-1032 The Korean Society for Molecular and Cellular Biology. All rights reserved. cc This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/. Mol. Cells 2020; 43(3): 215-221 215 Developmental Features of Olfactory Bulb Interneurons Jae Yeon Kim et al. discussed the recently identified mechanisms underlying OB and Sadikot, 2007). Interneurons with similar fates deter- interneurons development and their physiological functions. mined by their same birthdate assemble with each other to form laminar structures and cooperate in modulating the signal responses of excitatory neurons (Bartolini et al., 2013). AMAZING CELL TYPE: INTERNEURON For example, early- and late-born MGE-derived interneurons The mammalian brain contains dozens of distinct types of predominantly settled in infragranular layers and supragran- interneurons with very diverse morphologies, molecular ular layers of the neocortex, respectively (Ma et al., 2006; markers, electrophysiological properties and connectivity that Rymar and Sadikot, 2007), establishing distinct neuronal in- modulate and refine neuronal circuits (Bandler et al., 2017; nervated circuits. Furthermore, it has been reported that the Hu et al., 2017). Broadly, GABAergic cells in the forebrain are final positioning of interneuron was not determined by their classified based on their progenitor origins, and which has clonality or lineage, rather, it might be affected by birthdates been studied well in mice (Fertuzinhos et al., 2009; Hansen et or migration machinery (Mayer et al., 2015). However, inte- al., 2013). In the progenitor zones of the three subcortical re- grative studies on the temporal specifications of interneurons gions of the brain, the medial ganglionic eminence (MGE), the are still lacking. caudal ganglionic eminence (CGE), and the lateral ganglionic eminence (LGE), many inhibitory cell subtypes are produced DISTINCT CHARACTERISTICS OF THE OLFACTORY during embryonic stages and migrate along stereotyped BULB INTERNEURONS streams, then finally disperse throughout the forebrain. MGE and CGE-derived interneurons which are mainly generated The OB, like the cortex, striatum or hippocampus, is a recip- during embryonic days 11-15 predominantly migrate into ient of the massive generation of GABAergic interneurons the cortex, hippocampus, amygdala, and striatum, whereas from the telencephalon. Although each region shares com- LGE-derived interneurons, which are generated from mid mon features for interneuron development, OB has a few embryonic days 13.5-15.5 become the olfactory bulb (OB)- unique properties (Fig. 1): a) the OB has an extremely higher or striatum-interneurons (Bandler et al., 2017; Torigoe et al., proportion of interneurons (I) to excitatory neurons (E), at a 2016). To more detail, cortical interneurons are divided into 100:1 ratio, compared to other brain regions at a 1:5 ratio up to 50 different types, which are characterized by a combi- (Bayer, 1983). The reason for the high conserved ratio of nation of molecular markers or other intrinsic factors (Lim et OB interneurons remains a mystery; b) neurogenesis for OB al., 2018; Wamsley and Fishell, 2017). The subdivided regions interneurons occurs not only in the embryonic stages but of ganglionic eminence can generate more specialized and also in the adult stages. Cortical interneurons are primarily differentiated interneurons (Rubenstein et al., 1994). That is, produced from the MGE or CGE from embryonic days 9.5- these regional domains are specified by transcriptional factors 17.5. However, OB interneurons are continuously generated with a spatial bias for the generation of specific interneuron from the LGE or subventricular zone (SVZ) throughout life types (Puelles and Rubenstein, 1993). For instance, Nkx2.1 (Alvarez-Buylla et al., 2001). Specifically, approximately 73% highly expressed in MGE, determines MGE-derived cell fate, of the interneurons are generated from the SVZ during the and the MGE-derived cells become somatostatin (SST)- or postnatal first or second week, 25% are born during the parvalbumin (PV)-expressing interneurons. In the case of embryonic stage from the LGE (Bayer, 1983; Hinds, 1968), CGE, Pax6, Prox1, and Sp8 are predominantly expressed and and only 2% are generated from adult neurogenesis; and the CGE-derived cells become vasoactive intestinal peptide c) in the migration of LGE or SVZ-derived cells into the OB, (VIP)- or cholecystokinin (CCK)-expressing interneurons. the interneuron precursors (neuroblast) tangentially migrate These observations strongly indicate that spatial specification through the RMS (Lledo et al., 2008; Lois and Alvarez-Buylla, critically contributes to the diversification of interneurons. 1994; Mirich et al., 2002; Rall et al., 1966), whose distance is relatively very long. This implies that LGE- or SVZ-derived precursors might have distinct migratory machinery, unlike TIMELY DEVELOPMENT AS A DETERMINANT OF the MGE- or SGZ-derived precursors traveling short distances INTERNEURON DIVERSITY (Lepousez et al., 2015). Lastly, GABAergic interneurons in OB The temporally defined development of interneurons is also rarely express SST or PV, which are representative markers a key factor in the diverse specifications of interneurons (Kao in cortical or hippocampal interneurons, implying that the and Lee, 2010; Osterhout et al., 2014). The temporally de- molecular markers identified before are not sufficient to fully fined expression of CoupTF2 determines the cell fate of pro- define or understand the diversity of the OB interneurons. genitor cells derived from the MGE in SST- and PV-expressing Given these distinct developmental features of OB interneu- cortical interneurons (Hu et al., 2017). Even interneurons rons, different approaches or criteria should be considered to with the same molecular cell fates can form different func- analyze OB interneurons. tional circuits dependent on their temporally defined birth. In the hippocampus, early-born and late-born PV-expressing DIVERSITY OF OLFACTORY BULB INTERNEURONS basket cells form synapses with different subpopulations of pyramidal neurons in CA1 and play differential roles in mem- OB interneurons are grouped into four classes by their soma ory and learning (Donato et al., 2015). Especially, the timely locations (Nagayama et al., 2014) (Fig. 2). First, granule cells development of interneurons is more closely correlated with (GC) represent the most abundant populations (~94%) and their final positioning in the brain (Fairen et al., 1986; Rymar are highly heterogeneous in their morphologies, connectiv- 216 Mol. Cells 2020; 43(3): 215-221 Developmental Features of Olfactory Bulb Interneurons Jae Yeon Kim et al. Fig. 1. Distinct features of OB interneurons development. Developmental characteristics of OB interneurons. a) OB has a higher conserved ratio of interneurons (I; orange) to excitatory neurons (E; green). b) Neurogenesis of OB interneurons throughout life. The red graph indicates the production timeline of OB interneurons. The blue graph indicates that of cortical interneurons. c) Long migration from the SVZ into the OB. Left: The MGE (orange line) mainly produces cortical interneurons. They migrate longer than excitatory precursors (green line). Right: During the postnatal stage, OB interneurons are consistently generated from the SVZ and migrate a very long distance into the OB. Orange circles: early-born interneurons, Yellow circles: late-born interneurons. Fig. 2. Four classes of OB interneurons by their soma locations. Left: Representation of the OB layers. GL: glomerulus layer, EPL: external plexiform layer, MCL: mitral cell layer, GCL: granule cell layer. Right: PGC: periglomerulus cell (purple), EPL-IN: interneuron located in the EPL (blue), MCL-IN: interneuron located in the MCL (green), sGC: superficial granule cell (red), dGC: deep granule cell (yellow). A dominant developmental period is typeset in bold font. ity, and intrinsic factors (Lledo et al., 2008). In 1987, Greer (EPL). However, Type 3 cells have cell bodies located in the reported three morphological subpopulations of mouse OB superficial GCL (sGCL) or proximal MCL and extend their GCs through Golgi qualitative analyses (Greer, 1987). Spe- apical dendrites through the entire EPL. The differences in cifically, Type 2 cells have cell bodies in the deep granule cell soma location and the range of the extending dendrites in layer (dGCL) and extend their dendrites into the mitral cell each subpopulation suggest that they are distinct subtypes of layer (MCL) and lower layer of the external plexiform layer GCs with different functional circuits. One GC makes connec- Mol. Cells 2020; 43(3): 215-221 217 Developmental Features of Olfactory Bulb Interneurons Jae Yeon Kim et al. tions with about 200-300 mitral or tufted cells (TC), causing DIVERSITY OF OB INTERNEURONS CLASSIFIED BY dendro-dendritic inhibition (Burton, 2017; Price and Powell, TEMPORAL SPECIFICATION 1970). In particular, interneurons integrated into the sGCL form neural circuits with TC. In contrast, interneurons inte- Recent studies have reported that GCs having the largest grated into the dGCL form synaptic connections mainly with population of OB interneurons can be divided into two dis- mitral cells (MC) (Lemasson et al., 2005; Mori, 1987; Orona tinct populations by their birth dates, postnatal early- and et al., 1983). The distinct anatomical connectivity by the postnatal late-born interneurons. They have properties differ- depth of the GCL implies differential functionality, but little ent from each other in functional connectivity of their final is known about the physiological olfactory functions of each positioning and survival rates (Bovetti et al., 2007; Lemasson layer. In fact, different subtypes of OB GCs originate from et al., 2005; Tseng et al., 2017). For example, postnatal ear- regionally specified origins expressing specialized transcrip- ly-born interneurons are located in the sGCL and mainly form tional factors (Fujiwara and Cave, 2016). For instance, sGCs inhibitory circuits with excitatory TCs. In contrast, almost all are generated from dorsal SVZ and highly express Emx1, SP8, postnatal late-born interneurons are integrated into the dGCL and Pax6, whereas dGCs are born from the ventral SVZ and and form circuits mainly with excitatory MCs (Lemasson et express Gsh1/2 or Nkx2.1 (Fuentealba et al., 2015). Howev- al., 2005; Mori, 1987). Furthermore, excitatory TCs and MCs er, little is known about the precise diversification of GCs and are directly innervated into the brain without thalamus relay their physiological circuits. and transmit integrated olfactory information into different Second, periglomerular cells (PGC), accounting for 4% of regions. MCs project their axons into the entire piriform cor- the total OB interneurons and surrounding glomerulus, can tex, including the amygdala and entorhinal cortex, and their directly make connections with axons of olfactory sensory synapses with GCs display more plasticity from the sensory in- neurons (OSN) and dendrodendritic synapses with MCs or puts (Huang et al., 2016). TCs intensively project their axons TCs (Lledo and Valley, 2016). PGCs consist of three types, into the anterior olfactory nucleus. The MCs exhibit interme- tyrosine hydroxylase (TH)-, calbindin (CB)-, or calretinin diate-frequency firing, responding to relatively high concen- (CR)-expressing cells. Whereas the TH- and CB-expressing tration, whereas the TCs convey high-frequency firing with cells are predominantly born at embryonic days 12.5-15.5, shorter latency, responding to even low odor concentration CR-expressing cells are generated during the postnatal stage (Igarashi et al., 2012). These results indicate that the distinct (Batista-Brito et al., 2008). neuronal circuits between postnatal early- and late-born OB Third, EPL-interneurons, which account for only 2% of interneurons can be translated into differential functions in the total interneurons, are characterized by PV or corticotro- olfactory information processing (Muthusamy et al., 2017). pin-releasing hormone (CRH) (Garcia et al., 2014; Liu et Additionally, postnatal early-born interneurons can survive al., 2019). They are produced in the late embryonic to early until adulthood, but over 50% of the late-born interneurons postnatal stages (Batista-Brito et al., 2008). Of great inter- undergo cell death after they reach the OB (Petreanu and est, one EPL-interneuron connects with over 1,000 MCs or Alvarez-Buylla, 2002). These different properties indicate that TCs, although the occupying ratio of EPL-interneurons in the the OB GCs are diversified by their timely development into entire OB interneuron populations is extremely rare (Burton, distinct subtypes with distinct extrinsic or intrinsic profiles. 2017). Furthermore, EPL-interneurons weight their synapses more specifically to TCs than MCs (Liu et al., 2019). This sug- TIMELY ACTION OF MOLECULAR MACHINERY FOR gests that each interneuron contributes to a distinct circuit by DIVERSIFICATION OF OB INTERNEURONS forming its preferred synapses depending on the interneuron types. To better understand the diverse OB interneurons, research Lastly, glycoprotein 5T4-expressing interneurons are lo- on the molecular mechanisms underlying the diversification cated above the MCL and are consistently generated until of interneurons has been conducted. Olfactory input de- adulthood (Yoshihara et al., 2012). Although 5T4 knockout pendently expressed transcription factors, such as c-fos and mice displayed dysfunctions in the firing of excitatory TCs and Npas4, modulated the survival rate of postnatal early-born in- defective olfactory behaviors (Takahashi et al., 2016), little is terneurons and doublecortin (Dcx)-mediated structural devel- known about the precise characteristics of MCL-interneurons opment of OB GCs, respectively (Tseng et al., 2017; Yoshihara themselves. et al., 2014). In addition, a recent study identified the specific It is intriguing that the same progenitor regions in the VZ signaling in postnatal early-born interneurons that facilitated produce different types of interneurons depending on the the temporal development of early-born related circuits for developmental stages (Fig. 2). For example, TH-expressing regulating innate olfactory functions (Kim et al., 2020). Abel- PGCs are predominantly generated in cortical progenitor-pro- son tyrosine-protein kinase 1 (Abl1), a proto-oncogene in- ducing VZ cells (cortical-VZ) during embryonic days 12.5- volved in chronic myelogenous leukemia (Wang et al., 1984) 15.5. During development, cortical VZ gradually mature into is highly expressed in postnatal early-born OB interneurons dorsal V-SVZ where sGCs are mainly produced. This might be contributing to the stabilization of Dcx. This Abl1-mediated because of changes in the LGE lineage specification during Dcx stabilization provides the driving force moving postnatal embryonic days 13.5-15.5 (Fuentealba et al., 2015). Howev- early-born interneurons to form OB circuits regulating innate er, an integrative understanding of the diversity of OB inter- olfactory behaviors, such as the detection of or sensitivity to neurons is still lacking. odorants. These studies suggest that the differential profile between early-born or late-born OB interneurons is caused 218 Mol. Cells 2020; 43(3): 215-221 Developmental Features of Olfactory Bulb Interneurons Jae Yeon Kim et al. Fig. 3. Developmental factors identified for functional inhibitory circuits in OB. Schematic representation of the birthdate-order dependent interneuron final positioning in the OB. The X-axis represents the birthdate and the Y-axis represents the final positions from the SVZ to target layers in the OB. For the correct positioning, each neuron underlies the distinct molecular machinery. Postnatal early- born interneurons (green cell) have active Abl1-Dcx signaling as migratory machinery for integration into the sGCL (green layer). sGCL- specific circuits perform innate olfactory functions, such as detection or sensitivity. by distinct molecular machinery, such as the action of tran- thalamic relay (Kay and Sherman, 2007); 2) OB interneurons scription factors or Abl1-Dcx signaling, thereby playing a are continuously generated even during the adult stage distinct role in olfactory information processing (Fig. 3). For (Alvarez-Buylla et al., 2001). During the development of OB more advanced understating of the distinct features of OB in- interneurons, they are consistently exposed to various and terneurons or functional circuits, integrative studies on other unexpected sensory stimuli, implying that the diversity of OB molecular mechanisms should be further investigated. interneurons might be evolutionary evidence of their adap- tation to diverse environmental stimuli; and 3) despite the fact that there is a smaller odorant receptor repertoire than CONCLUSION AND PERSPECTIVES in other species, humans still can distinguish 1 trillion smells The OB interneurons are extremely abundant and diverse. (Bushdid et al., 2014; Zozulya et al., 2001). This suggests that Here, we pointed out the unique characteristics of OB there must be other machinery for odor discrimination in the interneurons different from other interneurons. Most no- central nervous system beyond odor sensing by the odorant tably, OB interneurons are generated over a long period receptors. Based on the above facts, it is expected that the from the mid-embryonic to the adult stage, and migrate a distinct developmental features of mouse OB interneurons long distance through the RMS into the OB. We also briefly might be conserved in human OB interneurons (Paredes et summarized that special molecular machinery, such sensory al., 2016; Zapiec et al., 2017). input-mediated c-fos synthesis and Abl1-Dcx signaling, is In summary, considering these unanswered and intriguing reflected in the unique properties of postnatal early-born in- questions about the diversity of OB interneurons, a deep fo- terneurons, including a high survival rate and integration into cus on these issues would be of crucial importance. Further- the sGCL forming the innate olfactory behaviors. Through more, it may provide new insights into cures for neurodevel- our review, we suggest that OB interneurons might be diver- opmental disorder patients having sensory hallucination. sified and clustered by a combination of their diverse and dis- tinct properties, including precursor origins, developmental Disclosure timing, sensory inputs, and migratory machinery. The authors have no potential conflicts of interest to disclose. Why OB interneurons are highly populated and diverse remains unsolved. This may be interpreted by some facts: 1) ACKNOWLEDGMENTS OB, as the first gating site of robust inputs from the external This research was supported by the Bio & Medical Tech- environment, tightly controls the E-I ratio (Anderson et al., nology Development Program of the National Research 2000; D’Amour and Froemke, 2015). Furthermore, it must Foundation (NRF) funded by the Korean government be associated with more tight or delicate modulation ma- (2017M3A9G8084463) and KBRI basic research program chinery, like interneurons, since the OB is a direct pathway through Korea Brain Research Institute funded by Ministry of for olfactory information processing to the cortex without Science and ICT (20-BR-04-01). Mol. Cells 2020; 43(3): 215-221 219 Developmental Features of Olfactory Bulb Interneurons Jae Yeon Kim et al. the autism spectrum. Perception 42, 341-355. ORCID Jae Yeon Kim https://orcid.org/0000-0002-0542-9071 Garcia, I., Quast, K.B., Huang, L., Herman, A.M., Selever, J., Deussing, J.M., Jiyun Choe https://orcid.org/0000-0002-1832-4818 Justice, N.J., and Arenkiel, B.R. (2014). Local CRH signaling promotes Cheil Moon https://orcid.org/0000-0002-9741-7229 synaptogenesis and circuit integration of adult-born neurons. Dev. Cell 30, 645-659. Gomes, E., Pedroso, F.S., and Wagner, M.B. (2008). 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Molecules and Cells – Pubmed Central
Published: Mar 17, 2020
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