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Sequential Pattern of Sublayer Formation in the Paleocortex and Neocortex

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Sequential Pattern of Sublayer Formation in the Paleocortex and Neocortex Medical Molecular Morphology (2020) 53:168–176 https://doi.org/10.1007/s00795-020-00245-7 ORIGINAL PAPER Sequential pattern of sublayer formation in the paleocortex and neocortex Makoto Nasu1 · Kenji Shimamura2 · Shigeyuki Esumi1 · Nobuaki Tamamaki1 Received: 17 December 2019 / Accepted: 13 January 2020 / Published online: 30 January 2020 © The Japanese Society for Clinical Molecular Morphology 2020 Abstract The piriform cortex (paleocortex) is the olfactory cortex or the primary cortex for the sense of smell. It receives the olfac- tory input from the mitral and tufted cells of the olfactory bulb and is involved in the processing of information pertaining to odors. The piriform cortex and the adjoining neocortex have diferent cytoarchitectures; while the former has a three-layered structure, the latter has a six-layered structure. The regulatory mechanisms underlying the building of the six-layered neo- cortex are well established; in contrast, less is known about of the regulatory mechanisms responsible for structure formation of the piriform cortex. The diferences as well as similarities in the regulatory mechanisms between the neocortex and the piriform cortex remain unclear. Here, the expression of neocortical layer-specifc genes in the piriform cortex was examined. Two sublayers were found to be distinguished in layer II of the piriform cortex using Ctip2/Bcl11b and Brn1/Pou3f3. The sequential expression pattern of Ctip2 and Brn1 in the piriform cortex was similar to that detected in the neocortex, although the laminar arrangement in the piriform cortex exhibited an outside-in arrangement, unlike that observed in the neocortex. Keywords Piriform cortex (paleocortex) · Sublayer · Sequential expression · Ctip2/Bcl11b · Brn1/Pou3f3 Introduction six-layered cortex, which is a mammal-specifc feature, are well established; sequential expression of transcription fac- The piriform cortex (paleocortex) is the olfactory cortex or tors is involved in determining cell identities, and late-born the primary cortex for the sense of smell. It receives the neurons migrate to pass through and take their place outside olfactory input from the mitral and tufted cells in the olfac- earlier-born neurons, i.e., in an inside-out manner [8–12]. tory bulb and is involved in the processing of information Recently, lineage trace analyses demonstrated that the pertaining to odors [1, 2]. Neurons originating from the lat- laminar organization of the piriform cortex is regulated in eral pallium (LP) in the telencephalon migrate laterally or an inside-out manner, while neurons located inside layer II ventrally into the piriform cortex [3, 4]. The dorsally adjoin- are arranged in an outside-in manner [13]. Furthermore, neu- ing dorsal pallium (DP) gives rise to the neocortex, which is rons in the superfcial and deeper layers of layer II, layers IIa responsible for higher mental functions, including memory, and IIb, respectively, exhibit diferent innervation patterns speech, value judgments, and sociality. The adjoining LP to other cortical regions [14, 15]. However, less is known and DP have diferent cytoarchitectures; LP is a three-lay- about the regulatory mechanisms in the piriform cortex. In ered structure, while DP is a six-layered structure [5–7]. particular, the diferences and similarities in the regulatory The regulatory mechanisms underlying the building of the mechanisms between the neocortex and the piriform cortex remain unclear, despite the fact that these two cortices are adjoined. * Makoto Nasu In this study, we examined the expression of some neo- [email protected] cortex layer-specifc genes in the piriform cortex at embry- 1 Department of Morphological Neural Science, Graduate onic day 16 (E16), postnatal day 0 (P0), and P7, which cor- School of Medical Sciences, Kumamoto University, 1-1-1, respond to the late-neurogenesis stage, the post-neurogenesis Honjo, Chuo-ku, Kumamoto 860-8556, Japan stage, and the postnatal developmental stage, respectively 2 Department of Brain Morphogenesis, Institute of Molecular [9]. Embryology and Genetics (IMEG), Kumamoto University, 2-2-1, Honjo, Chuo-ku, Kumamoto 860-0811, Japan Vol:.(1234567890)1 3 Medical Molecular Morphology (2020) 53:168–176 169 ab c d e f g h i j k l 1 3 170 Medical Molecular Morphology (2020) 53:168–176 ◂Fig. 1 Sublayers in layer II of the piriform cortex at P7. a Overview (FV-1200, FV-1000; OLYMPUS) and analyzed using the of the telencephalon at P7. The piriform cortex (Pir) adjoins the neo- ImageJ software. cortex (NCx) and the olfactory tubercle (Tu). Their borders are indi- cated by white dotted lines. Pir consists of three layers (I, II and III). NCx consists of six layers (I, II/III, IV, V and VI). b The piriform Image analysis cortex stained with Hoechst 33343. The endopiriform nucleus (EN) is located in the deeper region of the piriform cortex. c Sublayers of Four-colored fuorescent images of the piriform cortex were piriform layer II, IIa and IIb, which are roughly segregated by the cell density. The white dashed lines indicate the layer/sublayer borders. obtained from three individuals at P0 and P7 using a laser- d–f Triple immunostaining for Tbr1 (d), Ctip2 (e) and Brn1 (f). The scanning confocal microscope and split into separate color border between NCx and Pir is indicated by the white dotted line. g–i channels. The fuorescence intensity of three markers (Tbr1, Merged view of d–f. g Tbr1 (green) and Ctip2 (red). h Tbr1 (green) Ctip2 and Brn1) and Hoechst 33342 (nuclear staining) in and Brn1 (red). i Brn1 (green) and Ctip2 (red). j–l Magnifed view of g–i. Hoechst 33342 was used for counterstaining of nuclei (blue). piriform layers IIa and IIb was analyzed by line plot profl- The solid lines roughly indicate the range of each layer. The border ing using the ImageJ software. Two 250 µm-long lines were of layers IIa and IIb was defned by the border of expression of Brn1 arranged at the superfcial and deepest position of piriform LOT Lv and indicated by a crossing bar. lateral olfactory tract, lateral layer II. The number of fuorescence+ neurons was counted ventricle, St striatum. Scale bars, 1000 µm (a); 200 µm (b–l) on each line. The fuorescence intensities per one cell were averaged for each individual. Cut-of values were set to Materials and methods 10% of the peak values. Student’s t tests were conducted to compare the fuorescence intensities and proportions of Tissue preparation marker+ cells among Hoechst 33342+ cells between layers IIa and IIb. P < 0.05 (two-tailed) was considered signifcant Jcl:ICR mice were killed at E16, P0, and P7 (purchased from for all tests. CLEA Japan). All mice were anesthetized with medetomi- dine/midazolam/butorphanol tartrate/phosphate bufered saline (PBS) (fnal dose, 0.3 mg/kg of body weight; 4 mg/kg Results of body weight; and 5 mg/kg of body weight, respectively) and perfused from the left ventricle with iced 4% paraform- Sublayers in layer II of the piriform cortex at P7 aldehyde/PBS (pH 7.2). Brain tissues were extracted and postfxed with 4% paraformaldehyde/PBS (pH 7.2) for 1 h To investigate the differences and similarities in the (E16) or overnight (P0 and P7). Fixed tissues were cryopro- regulatory mechanisms between the neocortex and the tected in 15% sucrose/PBS overnight at 4 °C and embed- piriform cortex (paleocortex) (Fig. 1a, b), we studied the ded in Tissue-Tek O.C.T. compound (Sakura Finetek). All expression of neocortical layer-specific genes. First, we animal experiments were performed in accordance with determined which neocortical layer-specific genes were institutional (Kumamoto University) guidelines and were also expressed in the piriform cortex. We performed approved by the animal care and use committee of Kuma- immunostaining using P7 mice and examined how their moto University. expressions were in each piriform layers and sublayers (Fig. 1c). Tbr1, Ctip2/Bcl11b, and Brn1/Pou3f3 were expressed strongly in the piriform cortex (Fig. 1d–f). Tbr1 Immunostaining and Ctip2 were expressed throughout layer II, whereas Brn1 was mainly expressed in the deeper half of layer II Frozen tissues were coronally sliced at 12 µm. Antigen (Fig. 1g–l), indicating that layer II of the piriform cortex retrieval was achieved through heat treatment (105 °C, can be subcategorized into two sublayers: the superficial 5 min) in 10 mM citrate bufer (pH 6.0). The following layer IIa (Tbr1+ /Ctip2+ /Brn1−) and the deeper layer primary antibodies were used for immunohistochemistry IIb (Tbr1+ /Ctip2+ /Brn1+) using molecular markers. at the indicated dilutions: anti-Brn1/Pou3f3 (goat, 1:200; Tbr1 and Ctip2 were colocalized in a group in the deeper Santa Cruz), anti-Brn2/Pou3f2 (goat, 1:200; Santa Cruz), region of the piriform cortex, which might correspond to anti-Ctip2/Bcl11b (rat monoclonal, 1:3000; Abcam), anti- the endopiriform nucleus (EN) (Fig. 1g). Tbr1, Ctip2, and Foxp2 (goat, 1:100; Santa Cruz), anti-RORb (mouse, 1:500; Brn1 were widely detected in a subset of layer III neurons Perseus), anti-Satb2 (rabbit, 1:1000; Abcam), and anti-Tbr1 with various combinations. Brn2/Pou3f2, Satb2, Foxp2, (rabbit, 1:1000; Abcam). Fluorescence (Alexa Fluor 488, and RORb were sparsely detected in the piriform cortex; 594 and Cy5)-conjugated secondary antibodies were used therefore, they could not be considered representative (donkey, 1:2000; Jackson ImmunoResearch Inc.). Images markers of piriform layers (Fig. 2a–d). Faint expression were acquired using a BZ-X700 fuorescence microscope signals for Brn2/Pou3f2 were detected sparsely in lay- (Keyence) and a laser-scanning confocal microscope ers II and III, whereas Satb2 and Foxp2 were sparsely 1 3 Medical Molecular Morphology (2020) 53:168–176 171 abc defgh Fig. 2 Immunostaining of the piriform cortex and neocortex at P7. to deep orientation of the cortical tissue was shown in the upper to a–d Immunostaining of the piriform cortex.
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