Mol. Cells 2020; 43(3): 215~221  https://doi.org/10.14348/molcells.2020.0033
Distinct Developmental Features of Olfactory Bulb Interneurons
Jae Yeon Kim 1, Jiyun Choe 1, and Cheil Moon 1,2,3, *
1Department of Brain and Cognitive Sciences, Graduate School, Daegu Gyeongbuk Institute of Science and Technology, Daegu
42988, Korea, 2Convergence Research Advanced Centre for Olfaction, Daegu Gyeongbuk Institute of Science and Technology,
Daegu 42988, Korea, 3Korea Brain Research Institute, Daegu 41062, Korea
Received January 30, 2020; Revised February 27, 2020; Accepted March 2, 2020.; Published online March 17, 2020.
© Korean Society for Molecular and Cellular Biology. All rights reserved.

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/).
ABSTRACT
The olfactory bulb (OB) has an extremely higher proportion of interneurons innervating excitatory neurons than other brain regions, which is evolutionally conserved across species.Despite the abundance of OB interneurons, little is known about the diversification and physiological functions of OB interneurons compared to cortical interneurons. In this review, an overview of the general developmental process of interneurons from the angles of the spatial and temporal specifications was presented. Then, the distinct features shown exclusively in OB interneurons development and molecular machinery recently identified were discussed.Finally, we proposed an evolutionary meaning for the diversity of OB interneurons.
Keywords: development, diversity, interneuron, olfactory bulb, spatio-temporal specification
INTRODUCTION

Identification of the neuronal components in the brain provides important insight for understanding high-order and complicated behaviors, including logical thinking, emotional sensation, and interaction with external signals (Ramón y Cajal et al., 1988). Specifically, interneurons control neurotransmission by the intricate modulation of information processing (Bartolini et al., 2013; Paredes et al., 2016). To adapt these diverse neuronal functions, interneurons are developed into morphologically, molecularly, and electrophysiologically diverse subtypes and are continuously generated from embryonic to even adult stages (Bartolini et al., 2013; Batista-Brito and Fishell, 2009; Kepecs and Fishell, 2014). Malformation of the interneurons during early development can lead to neurodevelopmental disorders, such as autism spectrum disorder (ASD) and Tourette’s syndrome (Ashwin et al., 2014; Marco et al., 2011). Thus, defining neuronal properties and classifying the myriad of diverse interneurons are essential for understanding complex brain physiologies (Maccaferri and Lacaille, 2003), as well as neurodevelopmental disorders (Fang et al., 2014).

Mammalian OB express the most abundant and varied interneurons in the brain, but they have received little attention 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 al., 2008; Tonacci et al., 2017). Furthermore, the abnormal structural development of OB interneurons in the early stage induces olfactory impairments (Kim et al., 2020; Yoshihara et al., 2014). These facts indicated that research on the development of interneurons in the OB is critical and fundamental. In this review, we introduced the distinct characteristics of OB interneuron development by comparing them to the common developmental features of other interneurons. We also discussed the recently identified mechanisms underlying OB interneurons development and their physiological functions.

AMAZING CELL TYPE: INTERNEURON

The mammalian brain contains dozens of distinct types of interneurons with very diverse morphologies, molecular markers, electrophysiological properties and connectivity that modulate and refine neuronal circuits (Bandler et al., 2017; Hu et al., 2017). Broadly, GABAergic cells in the forebrain are classified based on their progenitor origins, and which has been studied well in mice (Fertuzinhos et al., 2009; Hansen et al., 2013). In the progenitor zones of the three subcortical regions of the brain, the medial ganglionic eminence (MGE), the caudal ganglionic eminence (CGE), and the lateral ganglionic eminence (LGE), many inhibitory cell subtypes are produced during embryonic stages and migrate along stereotyped streams, then finally disperse throughout the forebrain. MGE and CGE-derived interneurons which are mainly generated during embryonic days 11-15 predominantly migrate into the cortex, hippocampus, amygdala, and striatum, whereas LGE-derived interneurons, which are generated from mid embryonic days 13.5-15.5 become the olfactory bulb (OB)- or striatum-interneurons (Bandler et al., 2017; Torigoe et al., 2016). To more detail, cortical interneurons are divided into up to 50 different types, which are characterized by a combination of molecular markers or other intrinsic factors (Lim et al., 2018; Wamsley and Fishell, 2017). The subdivided regions of ganglionic eminence can generate more specialized and differentiated interneurons (Rubenstein et al., 1994). That is, these regional domains are specified by transcriptional factors with a spatial bias for the generation of specific interneuron types (Puelles and Rubenstein, 1993). For instance, Nkx2.1 highly expressed in MGE, determines MGE-derived cell fate, and the MGE-derived cells become somatostatin (SST)- or parvalbumin (PV)-expressing interneurons. In the case of CGE, Pax6, Prox1, and Sp8 are predominantly expressed and the CGE-derived cells become vasoactive intestinal peptide (VIP)- or cholecystokinin (CCK)-expressing interneurons. These observations strongly indicate that spatial specification critically contributes to the diversification of interneurons.

TIMELY DEVELOPMENT AS A DETERMINANT OF INTERNEURON DIVERSITY

The temporally defined development of interneurons is also a key factor in the diverse specifications of interneurons (Kao and Lee, 2010; Osterhout et al., 2014). The temporally defined expression of CoupTF2 determines the cell fate of progenitor cells derived from the MGE in SST- and PV-expressing cortical interneurons (Hu et al., 2017). Even interneurons with the same molecular cell fates can form different functional circuits dependent on their temporally defined birth. In the hippocampus, early-born and late-born PV-expressing basket cells form synapses with different subpopulations of pyramidal neurons in CA1 and play differential roles in memory and learning (Donato et al., 2015). Especially, the timely development of interneurons is more closely correlated with their final positioning in the brain (Fairen et al., 1986; Rymar and Sadikot, 2007). Interneurons with similar fates determined 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). For example, early- and late-born MGE-derived interneurons predominantly settled in infragranular layers and supragranular layers of the neocortex, respectively (Ma et al., 2006; Rymar and Sadikot, 2007), establishing distinct neuronal innervated circuits. Furthermore, it has been reported that the final positioning of interneuron was not determined by their clonality or lineage, rather, it might be affected by birthdates or migration machinery (Mayer et al., 2015). However, integrative studies on the temporal specifications of interneurons are still lacking.

DISTINCT CHARACTERISTICS OF THE OLFACTORY BULB INTERNEURONS

The OB, like the cortex, striatum or hippocampus, is a recipient of the massive generation of GABAergic interneurons from the telencephalon. Although each region shares common features for interneuron development, OB has a few unique properties (Fig. 1): a) the OB has an extremely higher proportion of interneurons (I) to excitatory neurons (E), at a 100:1 ratio, compared to other brain regions at a 1:5 ratio (Bayer, 1983). The reason for the high conserved ratio of OB interneurons remains a mystery; b) neurogenesis for OB interneurons occurs not only in the embryonic stages but also in the adult stages. Cortical interneurons are primarily produced from the MGE or CGE from embryonic days 9.5-17.5. However, OB interneurons are continuously generated from the LGE or subventricular zone (SVZ) throughout life (Alvarez-Buylla et al., 2001). Specifically, approximately 73% of the interneurons are generated from the SVZ during the postnatal first or second week, 25% are born during the embryonic stage from the LGE (Bayer, 1983; Hinds, 1968), and only 2% are generated from adult neurogenesis; and c) in the migration of LGE or SVZ-derived cells into the OB, the interneuron precursors (neuroblast) tangentially migrate through the RMS (Lledo et al., 2008; Lois and Alvarez-Buylla, 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 the MGE- or SGZ-derived precursors traveling short distances (Lepousez et al., 2015). Lastly, GABAergic interneurons in OB rarely express SST or PV, which are representative markers in cortical or hippocampal interneurons, implying that the molecular markers identified before are not sufficient to fully define or understand the diversity of the OB interneurons. Given these distinct developmental features of OB interneurons, different approaches or criteria should be considered to analyze OB interneurons.

DIVERSITY OF OLFACTORY BULB INTERNEURONS

OB interneurons are grouped into four classes by their soma locations (Nagayama et al., 2014) (Fig. 2). First, granule cells (GC) represent the most abundant populations (~94%) and are highly heterogeneous in their morphologies, connectivity, and intrinsic factors (Lledo et al., 2008). In 1987, Greer reported three morphological subpopulations of mouse OB GCs through Golgi qualitative analyses (Greer, 1987). Specifically, Type 2 cells have cell bodies in the deep granule cell layer (dGCL) and extend their dendrites into the mitral cell layer (MCL) and lower layer of the external plexiform layer (EPL). However, Type 3 cells have cell bodies located in the superficial GCL (sGCL) or proximal MCL and extend their apical dendrites through the entire EPL. The differences in soma location and the range of the extending dendrites in each subpopulation suggest that they are distinct subtypes of GCs with different functional circuits. One GC makes connections with about 200-300 mitral or tufted cells (TC), causing dendro-dendritic inhibition (Burton, 2017; Price and Powell, 1970). In particular, interneurons integrated into the sGCL form neural circuits with TC. In contrast, interneurons integrated into the dGCL form synaptic connections mainly with mitral cells (MC) (Lemasson et al., 2005; Mori, 1987; Orona et al., 1983). The distinct anatomical connectivity by the depth of the GCL implies differential functionality, but little is known about the physiological olfactory functions of each layer. In fact, different subtypes of OB GCs originate from regionally specified origins expressing specialized transcriptional factors (Fujiwara and Cave, 2016). For instance, sGCs are generated from dorsal SVZ and highly express Emx1, SP8, and Pax6, whereas dGCs are born from the ventral SVZ and express Gsh1/2 or Nkx2.1 (Fuentealba et al., 2015). However, little is known about the precise diversification of GCs and their physiological circuits.

Second, periglomerular cells (PGC), accounting for 4% of the total OB interneurons and surrounding glomerulus, can directly make connections with axons of olfactory sensory neurons (OSN) and dendrodendritic synapses with MCs or TCs (Lledo and Valley, 2016). PGCs consist of three types, tyrosine hydroxylase (TH)-, calbindin (CB)-, or calretinin (CR)-expressing cells. Whereas the TH- and CB-expressing cells are predominantly born at embryonic days 12.5-15.5, CR-expressing cells are generated during the postnatal stage (Batista-Brito et al., 2008).

Third, EPL-interneurons, which account for only 2% of the total interneurons, are characterized by PV or corticotropin-releasing hormone (CRH) (Garcia et al., 2014; Liu et al., 2019). They are produced in the late embryonic to early postnatal stages (Batista-Brito et al., 2008). Of great interest, one EPL-interneuron connects with over 1,000 MCs or TCs, although the occupying ratio of EPL-interneurons in the entire OB interneuron populations is extremely rare (Burton, 2017). Furthermore, EPL-interneurons weight their synapses more specifically to TCs than MCs (Liu et al., 2019). This suggests that each interneuron contributes to a distinct circuit by forming its preferred synapses depending on the interneuron types.

Lastly, glycoprotein 5T4-expressing interneurons are located above the MCL and are consistently generated until adulthood (Yoshihara et al., 2012). Although 5T4 knockout mice displayed dysfunctions in the firing of excitatory TCs and defective olfactory behaviors (Takahashi et al., 2016), little is known about the precise characteristics of MCL-interneurons themselves.

It is intriguing that the same progenitor regions in the VZ produce different types of interneurons depending on the developmental stages (Fig. 2). For example, TH-expressing PGCs are predominantly generated in cortical progenitor-producing VZ cells (cortical-VZ) during embryonic days 12.5-15.5. During development, cortical VZ gradually mature into dorsal V-SVZ where sGCs are mainly produced. This might be because of changes in the LGE lineage specification during embryonic days 13.5-15.5 (Fuentealba et al., 2015). However, an integrative understanding of the diversity of OB interneurons is still lacking.

DIVERSITY OF OB INTERNEURONS CLASSIFIED BY TEMPORAL SPECIFICATION

Recent studies have reported that GCs having the largest population of OB interneurons can be divided into two distinct populations by their birth dates, postnatal early- and postnatal late-born interneurons. They have properties different from each other in functional connectivity of their final positioning and survival rates (Bovetti et al., 2007; Lemasson et al., 2005; Tseng et al., 2017). For example, postnatal early-born interneurons are located in the sGCL and mainly form inhibitory circuits with excitatory TCs. In contrast, almost all postnatal late-born interneurons are integrated into the dGCL and form circuits mainly with excitatory MCs (Lemasson et al., 2005; Mori, 1987). Furthermore, excitatory TCs and MCs are directly innervated into the brain without thalamus relay and transmit integrated olfactory information into different regions. MCs project their axons into the entire piriform cortex, including the amygdala and entorhinal cortex, and their synapses with GCs display more plasticity from the sensory inputs (Huang et al., 2016). TCs intensively project their axons into the anterior olfactory nucleus. The MCs exhibit intermediate-frequency firing, responding to relatively high concentration, whereas the TCs convey high-frequency firing with shorter latency, responding to even low odor concentration (Igarashi et al., 2012). These results indicate that the distinct neuronal circuits between postnatal early- and late-born OB interneurons can be translated into differential functions in olfactory information processing (Muthusamy et al., 2017). Additionally, postnatal early-born interneurons can survive until adulthood, but over 50% of the late-born interneurons undergo cell death after they reach the OB (Petreanu and Alvarez-Buylla, 2002). These different properties indicate that the OB GCs are diversified by their timely development into distinct subtypes with distinct extrinsic or intrinsic profiles.

TIMELY ACTION OF MOLECULAR MACHINERY FOR DIVERSIFICATION OF OB INTERNEURONS

To better understand the diverse OB interneurons, research on the molecular mechanisms underlying the diversification of interneurons has been conducted. Olfactory input dependently expressed transcription factors, such as c-fos and Npas4, modulated the survival rate of postnatal early-born interneurons and doublecortin (Dcx)-mediated structural development of OB GCs, respectively (Tseng et al., 2017; Yoshihara et al., 2014). In addition, a recent study identified the specific signaling in postnatal early-born interneurons that facilitated the temporal development of early-born related circuits for regulating innate olfactory functions (Kim et al., 2020). Abelson tyrosine-protein kinase 1 (Abl1), a proto-oncogene involved in chronic myelogenous leukemia (Wang et al., 1984) is highly expressed in postnatal early-born OB interneurons contributing to the stabilization of Dcx. This Abl1-mediated Dcx stabilization provides the driving force moving postnatal early-born interneurons to form OB circuits regulating innate olfactory behaviors, such as the detection of or sensitivity to odorants. These studies suggest that the differential profile between early-born or late-born OB interneurons is caused by distinct molecular machinery, such as the action of transcription factors or Abl1-Dcx signaling, thereby playing a distinct role in olfactory information processing (Fig. 3). For more advanced understating of the distinct features of OB interneurons or functional circuits, integrative studies on other molecular mechanisms should be further investigated.

CONCLUSION AND PERSPECTIVES

The OB interneurons are extremely abundant and diverse. Here, we pointed out the unique characteristics of OB interneurons different from other interneurons. Most notably, OB interneurons are generated over a long period from the mid-embryonic to the adult stage, and migrate a long distance through the RMS into the OB. We also briefly summarized that special molecular machinery, such sensory input-mediated c-fos synthesis and Abl1-Dcx signaling, is reflected in the unique properties of postnatal early-born interneurons, including a high survival rate and integration into the sGCL forming the innate olfactory behaviors. Through our review, we suggest that OB interneurons might be diversified and clustered by a combination of their diverse and distinct properties, including precursor origins, developmental timing, sensory inputs, and migratory machinery.

Why OB interneurons are highly populated and diverse remains unsolved. This may be interpreted by some facts: 1) OB, as the first gating site of robust inputs from the external environment, tightly controls the E-I ratio (Anderson et al., 2000; D’Amour and Froemke, 2015). Furthermore, it must be associated with more tight or delicate modulation machinery, like interneurons, since the OB is a direct pathway for olfactory information processing to the cortex without thalamic relay (Kay and Sherman, 2007); 2) OB interneurons are continuously generated even during the adult stage (Alvarez-Buylla et al., 2001). During the development of OB interneurons, they are consistently exposed to various and unexpected sensory stimuli, implying that the diversity of OB interneurons might be evolutionary evidence of their adaptation to diverse environmental stimuli; and 3) despite the fact that there is a smaller odorant receptor repertoire than in other species, humans still can distinguish 1 trillion smells (Bushdid et al., 2014; Zozulya et al., 2001). This suggests that there must be other machinery for odor discrimination in the central nervous system beyond odor sensing by the odorant receptors. Based on the above facts, it is expected that the distinct developmental features of mouse OB interneurons might be conserved in human OB interneurons (Paredes et al., 2016; Zapiec et al., 2017).

In summary, considering these unanswered and intriguing questions about the diversity of OB interneurons, a deep focus on these issues would be of crucial importance. Furthermore, it may provide new insights into cures for neurodevelopmental disorder patients having sensory hallucination.

Disclosure

The authors have no potential conflicts of interest to disclose.

ACKNOWLEDGMENTS

This research was supported by the Bio & Medical Technology Development Program of the National Research Foundation (NRF) funded by the Korean government (2017M3A9G8084463) and KBRI basic research program through Korea Brain Research Institute funded by Ministry of Science and ICT (20-BR-04-01).

FIGURES
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.
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.
REFERENCES
  1. Alvarez-Buylla, A., Garcia-Verdugo, J.M., and Tramontin, A.D. (2001). A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287-293.
    Pubmed CrossRef
  2. Anderson, J.S., Carandini, M., and Ferster, D. (2000). Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926.
    Pubmed CrossRef
  3. Ashwin, C., Chapman, E., Howells, J., Rhydderch, D., Walker, I., and Baron-Cohen, S. (2014). Enhanced olfactory sensitivity in autism spectrum conditions. Mol. Autism 5, 53.
    Pubmed KoreaMed CrossRef
  4. Bandler, R.C., Mayer, C., and Fishell, G. (2017). Cortical interneuron specification: the juncture of genes, time and geometry. Curr. Opin. Neurobiol. 42, 17-24.
    Pubmed KoreaMed CrossRef
  5. Bartolini, G., Ciceri, G., and Marin, O. (2013). Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults. Neuron 79, 849-864.
    Pubmed CrossRef
  6. Batista-Brito, R., Close, J., Machold, R., and Fishell, G. (2008). The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 28, 3966-3975.
    Pubmed KoreaMed CrossRef
  7. Batista-Brito, R., and Fishell, G. (2009). The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87, 81-118.
    Pubmed KoreaMed CrossRef
  8. Bayer, S.A. (1983). 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329-340.
    Pubmed CrossRef
  9. Bovetti, S., Peretto, P., Fasolo, A., and De Marchis, S. (2007). Spatio-temporal specification of olfactory bulb interneurons. J. Mol. Histol. 38, 563-569.
    Pubmed CrossRef
  10. Burton, S.D. (2017). Inhibitory circuits of the mammalian main olfactory bulb. J. Neurophysiol. 118, 2034-2051.
    Pubmed KoreaMed CrossRef
  11. Bushdid, C., Magnasco, M.O., Vosshall, L.B., and Keller, A. (2014). Humans can discriminate more than 1 trillion olfactory stimuli. Science 343, 1370-1372.
    Pubmed KoreaMed CrossRef
  12. D'Amour, J.A., and Froemke, R.C. (2015). Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex. Neuron 86, 514-528.
    Pubmed KoreaMed CrossRef
  13. Donato, F., Chowdhury, A., Lahr, M., and Caroni, P. (2015). Early- and late-born parvalbumin basket cell subpopulations exhibiting distinct regulation and roles in learning. Neuron 85, 770-786.
    Pubmed CrossRef
  14. Fairen, A., Cobas, A., and Fonseca, M. (1986). Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J. Comp. Neurol. 251, 67-83.
    Pubmed CrossRef
  15. Fang, W.Q., Chen, W.W., Jiang, L., Liu, K., Yung, W.H., Fu, A.K.Y., and Ip, N.Y. (2014). Overproduction of upper-layer neurons in the neocortex leads to autism-like features in mice. Cell Rep. 9, 1635-1643.
    Pubmed CrossRef
  16. Fertuzinhos, S., Krsnik, Z., Kawasawa, Y.I., Rasin, M.R., Kwan, K.Y., Chen, J.G., Judas, M., Hayashi, M., and Sestan, N. (2009). Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia. Cereb. Cortex 19, 2196-2207.
    Pubmed KoreaMed CrossRef
  17. Fuentealba, L.C., Rompani, S.B., Parraguez, J.I., Obernier, K., Romero, R., Cepko, C.L., and Alvarez-Buylla, A. (2015). Embryonic origin of postnatal neural stem cells. Cell 161, 1644-1655.
    Pubmed KoreaMed CrossRef
  18. Fujiwara, N., and Cave, J.W. (2016). Partial conservation between mice and humans in olfactory bulb interneuron transcription factor codes. Front. Neurosci. 10, 337.
    Pubmed KoreaMed CrossRef
  19. Galle, S.A., Courchesne, V., Mottron, L., and Frasnelli, J. (2013). Olfaction in the autism spectrum. Perception 42, 341-355.
    Pubmed CrossRef
  20. Garcia, I., Quast, K.B., Huang, L., Herman, A.M., Selever, J., Deussing, J.M., Justice, N.J., and Arenkiel, B.R. (2014). Local CRH signaling promotes synaptogenesis and circuit integration of adult-born neurons. Dev. Cell 30, 645-659.
    Pubmed KoreaMed CrossRef
  21. Gomes, E., Pedroso, F.S., and Wagner, M.B. (2008). Auditory hypersensitivity in the autistic spectrum disorder. Pro Fono 20, 279-284.
    Pubmed CrossRef
  22. Greer, C.A. (1987). Golgi analyses of dendritic organization among denervated olfactory bulb granule cells. J. Comp. Neurol. 257, 442-452.
    Pubmed CrossRef
  23. Hansen, D.V., Lui, J.H., Flandin, P., Yoshikawa, K., Rubenstein, J.L., Alvarez-Buylla, A., and Kriegstein, A.R. (2013). Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat. Neurosci. 16, 1576-1587.
    Pubmed KoreaMed CrossRef
  24. Hinds, J.W. (1968). Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J. Comp. Neurol. 134, 287-304.
    Pubmed CrossRef
  25. Hu, J.S., Vogt, D., Sandberg, M., and Rubenstein, J.L. (2017). Cortical interneuron development: a tale of time and space. Development 144, 3867-3878.
    Pubmed KoreaMed CrossRef
  26. Huang, L., Ung, K., Garcia, I., Quast, K.B., Cordiner, K., Saggau, P., and Arenkiel, B.R. (2016). Task learning promotes plasticity of interneuron connectivity maps in the olfactory bulb. J. Neurosci. 36, 8856-8871.
    Pubmed KoreaMed CrossRef
  27. Igarashi, K.M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W.R., et al. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985.
    Pubmed KoreaMed CrossRef
  28. Kao, C.F., and Lee, T. (2010). Birth time/order-dependent neuron type specification. Curr. Opin. Neurobiol. 20, 14-21.
    Pubmed KoreaMed CrossRef
  29. Kay, L.M., and Sherman, S.M. (2007). An argument for an olfactory thalamus. Trends Neurosci. 30, 47-53.
    Pubmed CrossRef
  30. Kepecs, A., and Fishell, G. (2014). Interneuron cell types are fit to function. Nature 505, 318-326.
    Pubmed KoreaMed CrossRef
  31. Kim, J.Y., Cho, B., and Moon, C. (2020). Timely inhibitory circuit formation controlled by Abl1 regulates innate olfactory behaviors in mouse. Cell Rep. 30, 187-201.
    Pubmed CrossRef
  32. Lemasson, M., Saghatelyan, A., Olivo-Marin, J.C., and Lledo, P.M. (2005). Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 25, 6816-6825.
    Pubmed KoreaMed CrossRef
  33. Lepousez, G., Nissant, A., and Lledo, P.M. (2015). Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86, 387-401.
    Pubmed CrossRef
  34. Lim, L., Mi, D., Llorca, A., and Marin, O. (2018). Development and functional diversification of cortical interneurons. Neuron 100, 294-313.
    Pubmed KoreaMed CrossRef
  35. Liu, G., Froudarakis, E., Patel, J.M., Kochukov, M.Y., Pekarek, B., Hunt, P.J., Patel, M., Ung, K., Fu, C.H., Jo, J., et al. (2019). Target specific functions of EPL interneurons in olfactory circuits. Nat. Commun. 10, 3369.
    Pubmed KoreaMed CrossRef
  36. Lledo, P.M., Merkle, F.T., and Alvarez-Buylla, A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31, 392-400.
    Pubmed KoreaMed CrossRef
  37. Lledo, P.M., and Valley, M. (2016). Adult olfactory bulb neurogenesis. Cold Spring Harb. Perspect. Biol. 8, a018945.
    Pubmed KoreaMed CrossRef
  38. Lois, C., and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
    Pubmed CrossRef
  39. Ma, Y., Hu, H., Berrebi, A.S., Mathers, P.H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082.
    Pubmed KoreaMed CrossRef
  40. Maccaferri, G., and Lacaille, J.C. (2003). Interneuron diversity series: hippocampal interneuron classifications--making things as simple as possible, not simpler. Trends Neurosci. 26, 564-571.
    Pubmed CrossRef
  41. Marco, E.J., Hinkley, L.B., Hill, S.S., and Nagarajan, S.S. (2011). Sensory processing in autism: a review of neurophysiologic findings. Pediatr. Res. 69(5 Pt 2), 48R-54R.
    Pubmed KoreaMed CrossRef
  42. Mayer, C., Jaglin, X.H., Cobbs, L.V., Bandler, R.C., Streicher, C., Cepko, C.L., Hippenmeyer, S., and Fishell, G. (2015). Clonally related forebrain interneurons disperse broadly across both functional areas and structural boundaries. Neuron 87, 989-998.
    Pubmed KoreaMed CrossRef
  43. Mirich, J.M., Williams, N.C., Berlau, D.J., and Brunjes, P.C. (2002). Comparative study of aging in the mouse olfactory bulb. J. Comp. Neurol. 454, 361-372.
    Pubmed CrossRef
  44. Mori, K. (1987). Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol. 29, 275-320.
    Pubmed CrossRef
  45. Muthusamy, N., Zhang, X., Johnson, C.A., Yadav, P.N., and Ghashghaei, H.T. (2017). Developmentally defined forebrain circuits regulate appetitive and aversive olfactory learning. Nat. Neurosci. 20, 20-23.
    Pubmed KoreaMed CrossRef
  46. Nagayama, S., Homma, R., and Imamura, F. (2014). Neuronal organization of olfactory bulb circuits. Front. Neural Circuits 8, 98.
    Pubmed KoreaMed CrossRef
  47. Orona, E., Scott, J.W., and Rainer, E.C. (1983). Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb. J. Comp. Neurol. 217, 227-237.
    Pubmed CrossRef
  48. Osterhout, J.A., El-Danaf, R.N., Nguyen, P.L., and Huberman, A.D. (2014). Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. Cell Rep. 8, 1006-1017.
    Pubmed KoreaMed CrossRef
  49. Paredes, M.F., James, D., Gil-Perotin, S., Kim, H., Cotter, J.A., Ng, C., Sandoval, K., Rowitch, D.H., Xu, D., McQuillen, P.S., et al. (2016). Extensive migration of young neurons into the infant human frontal lobe. Science 354, aaf7073.
    Pubmed KoreaMed CrossRef
  50. Petreanu, L., and Alvarez-Buylla, A. (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106-6113.
    Pubmed KoreaMed CrossRef
  51. Price, J.L., and Powell, T.P. (1970). The morphology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 91-123.
    Pubmed
  52. Puelles, L., and Rubenstein, J.L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16, 472-479.
    Pubmed CrossRef
  53. Rall, W., Shepherd, G.M., Reese, T.S., and Brightman, M.W. (1966). Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44-56.
    Pubmed CrossRef
  54. Ramón y Cajal, S., DeFelipe, J., and Jones, E.G. (1988). Cajal on the Cerebral Cortex: An Annotated Translation of the Complete Writings (New York: Oxford University Press).
  55. Rubenstein, J.L., Martinez, S., Shimamura, K., and Puelles, L. (1994). The embryonic vertebrate forebrain: the prosomeric model. Science 266, 578-580.
    Pubmed CrossRef
  56. Rymar, V.V., and Sadikot, A.F. (2007). Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype. J. Comp. Neurol. 501, 369-380.
    Pubmed CrossRef
  57. Takahashi, H., Ogawa, Y., Yoshihara, S., Asahina, R., Kinoshita, M., Kitano, T., Kitsuki, M., Tatsumi, K., Okuda, M., Tatsumi, K., et al. (2016). A subtype of olfactory bulb interneurons is required for odor detection and discrimination behaviors. J. Neurosci. 36, 8210-8227.
    Pubmed KoreaMed CrossRef
  58. Tonacci, A., Billeci, L., Tartarisco, G., Ruta, L., Muratori, F., Pioggia, G., and Gangemi, S. (2017). [Formula: see text]Olfaction in autism spectrum disorders: a systematic review. Child Neuropsychol. 23, 1-25.
    Pubmed CrossRef
  59. Torigoe, M., Yamauchi, K., Kimura, T., Uemura, Y., and Murakami, F. (2016). Evidence that the laminar fate of LGE/CGE-derived neocortical interneurons is dependent on their progenitor domains. J. Neurosci. 36, 2044-2056.
    Pubmed KoreaMed CrossRef
  60. Tseng, C.S., Chao, H.W., Huang, H.S., and Huang, Y.S. (2017). Olfactory-experience- and developmental-stage-dependent control of CPEB4 regulates c-Fos mRNA translation for granule cell survival. Cell Rep. 21, 2264-2276.
    Pubmed CrossRef
  61. Wamsley, B., and Fishell, G. (2017). Genetic and activity-dependent mechanisms underlying interneuron diversity. Nat. Rev. Neurosci. 18, 299-309.
    Pubmed CrossRef
  62. Wang, J.Y., Ledley, F., Goff, S., Lee, R., Groner, Y., and Baltimore, D. (1984). The mouse c-abl locus: molecular cloning and characterization. Cell 36, 349-356.
    Pubmed CrossRef
  63. Yoshihara, S., Takahashi, H., Nishimura, N., Kinoshita, M., Asahina, R., Kitsuki, M., Tatsumi, K., Furukawa-Hibi, Y., Hirai, H., Nagai, T., et al. (2014). Npas4 regulates Mdm2 and thus Dcx in experience-dependent dendritic spine development of newborn olfactory bulb interneurons. Cell Rep. 8, 843-857.
    Pubmed CrossRef
  64. Yoshihara, S., Takahashi, H., Nishimura, N., Naritsuka, H., Shirao, T., Hirai, H., Yoshihara, Y., Mori, K., Stern, P.L., and Tsuboi, A. (2012). 5T4 glycoprotein regulates the sensory input-dependent development of a specific subtype of newborn interneurons in the mouse olfactory bulb. J. Neurosci. 32, 2217-2226.
    Pubmed KoreaMed CrossRef
  65. Zapiec, B., Dieriks, B.V., Tan, S., Faull, R.L.M., Mombaerts, P., and Curtis, M.A. (2017). A ventral glomerular deficit in Parkinson's disease revealed by whole olfactory bulb reconstruction. Brain 140, 2722-2736.
    Pubmed KoreaMed CrossRef
  66. Zozulya, S., Echeverri, F., and Nguyen, T. (2001). The human olfactory receptor repertoire. Genome Biol. 2, RESEARCH0018.
    Pubmed KoreaMed CrossRef


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