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WIREs Dev Biol
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Development of the thalamus: From early patterning to regulation of cortical functions

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Abstract The thalamus is a brain structure of the vertebrate diencephalon that plays a central role in regulating diverse functions of the cerebral cortex. In traditional view of vertebrate neuroanatomy, the thalamus includes three regions, dorsal thalamus, ventral thalamus, and epithalamus. Recent molecular embryological studies have redefined the thalamus and the associated axial nomenclature of the diencephalon in the context of forebrain patterning. This new view has provided a useful conceptual framework for studies on molecular mechanisms of patterning, neurogenesis and fate specification in the thalamus as well as the guidance mechanisms for thalamocortical axons. Additionally, the availability of genetic tools in mice has led to important findings on how thalamic development is linked to the development of other brain regions, particularly the cerebral cortex. This article will give an overview of the organization of the embryonic thalamus and how progenitor cells in the thalamus generate neurons that are organized into discrete nuclei. I will then discuss how thalamic development is orchestrated with the development of the cerebral cortex and other brain regions. This article is categorized under: Nervous System Development > Vertebrates: Regional Development Nervous System Development > Vertebrates: General Principles
Position of the thalamus in the forebrain. A and B are parasagittal sections of E11.5 mouse forebrain stained with an antibody against the bHLH protein OLIG3 (magenta). (a) Columnar model of the forebrain organization. In this traditional model, the dorsal (D)‐ventral (V) axis is perpendicular to the base of the brain. As a result, the thalamus (denoted as the “dorsal thalamus” in this model) is located dorsal to the prethalamus (denoted as the “ventral thalamus”). (b) Prosomere model of the forebrain organization. The anterior (A)‐posterior (P) or the rostro‐caudal axis matches the true border between the basal and alar plates that is defined by the expression of specific genes (e.g., Nkx2.2) induced by the ventralizing signal, sonic hedgehog (SHH). The thalamus is located caudal to the prethalamus, and the zona limitans intrathalamica (ZLI) is between the thalamus and the prethalamus. (c) A schematic view of the diencephalic prosomeres. Prosomere 1 (p1) is most caudally located and it includes the pretectum in its alar portion. Prosomere 2 (p2) is rostral to P1 and includes the thalamus and habenula in its alar portion. Prosomere 3 (p3) is most rostrally located and includes the prethalamus and eminentia thalami in its alar portion. (d) The frontal section of the forebrain showing the location of the thalamus (green; expressing OLIG3) and the ZLI (magenta; expressing SHH and OLIG3). The plain of section for D is shown in C as a purple dotted line
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Proliferation and differentiation of individual neural progenitor cells in the thalamus. (a) Three models of nuclear fate specification in early progenitor cells in the pTH‐C domain of the thalamus. a1. Nuclear fate in each thalamic progenitor cell is already specified so that each cell produces neurons that populate only a single nucleus at a late stage. a2. Nuclear fate in each thalamic progenitor cell is not yet specified so that each cell produces neurons that populate any thalamic nuclei at a late stage. a3. Nuclear fate in each thalamic progenitor cell is partially specified so that each cell produces neurons that populate a subset of nuclei at a late stage. Clonal lineage tracing supports this model in which individual radial glia contributes to a group of nuclei that are aligned in a radial order. (b) Patterns of cell division inferred from clonal lineage tracing studies. On average, individual radial glial cell that divides asymmetrically generates about a dozen neurons. b1. Rostroventrally located radial glia produce neurons of principal sensory nuclei in early rounds of cell division. Later in development, they produce neurons that populate more medially located thalamic nuclei. b2. Caudodorsally located radial glia produce neurons of laterally located, nonprincipal sensory nuclei in early rounds of cell division. Later in development, they produce neurons that populate more medially located thalamic nuclei
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Progenitor domains of the thalamus during neurogenesis. (a) A schematic, parasagittal view of the mouse diencephalon based on the prosomeric model. The dotted line indicates the plain of section shown in B. The green line is the border between the alar plate and the basal plate. The thalamus is included in prosomere 2 (P2). (b) During neurogenesis in early embryos, the thalamus consists of two progenitor domains, pTH‐C (green) and pTH‐R (brown). The ZLI (blue) is rostral to the pTH‐R domain and forms the border between the thalamus and the prethalamus (PTh). The pretectum (PT) is located just caudal to the pTH‐C domain. At the population level, the pTH‐C domain gives rise to the part of the thalamus that has reciprocal connections with the cerebral cortex. The rostral part of the pTH‐C domain (shown in dark green) close to pTH‐R preferentially contributes to principal sensory nuclei and other nuclei that are located medial to the principal sensory nuclei. The caudal part of the pTH‐C domain (shown in light green) close to the pretectum preferentially gives rise to caudodorsally located thalamic nuclei. The pTH‐R domain contributes to two nuclei in the thalamus (intergeniculate leaflet; IGL and lateral part of the ventral lateral geniculate (vLG) that are occupied by GABAergic inhibitory neurons. This domain also contributes to some GABAergic neurons of the pretectum. (c) Marker expression in thalamic progenitor domains. OLIG3 (orange) is expressed in both pTH‐C and pTH‐R domains as well as in the ZLI. ASCL1, HELT, and NKX2.2 (brown) are expressed in the pTH‐R but not in the pTH‐C domain. SHH and FOXA2 (blue) are expressed in the ZLI. NEUROG1 and NEUROG2 (green, blue) are expressed in the pTH‐C domain and the ZLI. OLIG2 is expressed in a graded pattern within the pTH‐C domain, with a higher expression toward the pTH‐C/pTH‐R border. DBX1 is expressed in an opposite gradient within the pTH‐C domain. There are also markers for early postmitotic cells derived from pTH‐C (Gbx2) or pTH‐R (Gata2, Gata3, Sox14, Tal1) progenitor domain. (d) Organization of mature thalamic nuclei. Color gradients approximately correspond to the originating progenitor domains shown in B. Schematics of three representative frontal sections are shown. Axis orientations are defined so that they correspond to those that define embryonic progenitor domains. AD, anterodorsal nucleus; AV, anteroventral nucleus; AM, anteromedial nucleus; Re, reuniens nucleus; MD, mediodorsal nucleus; PV, paraventricular nucleus; PT, pretectum; LP, lateral posterior nucleus; dLG, dorsal lateral geniculate nucleus; Po, posterior nucleus; PF, parafascicular nucleus; VPM, ventral posteromedial nucleus; VPL, ventral posterolateral nucleus; IGL, intergeniculate leaflet; vLG, ventral lateral geniculate nucleus; ZI, zona incerta; MGd, medial geniculate nucleus (dorsal part); MGv, medial geniculate nucleus (ventral part)
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