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Boundary Formation and Compartition in the Avian Diencephalon

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Boundary Formation and Compartition in the Avian Diencephalon The Journal of Neuroscience, July 1, 2001, 21(13):4699–4711 Boundary Formation and Compartition in the Avian Diencephalon Camilla W. Larsen, Lori M. Zeltser, and Andrew Lumsden Medical Research Council Centre for Developmental Neurobiology, King’s College London, London SE1 1UL, England The diencephalon comprises three functionally distinct regions: boundary does not. Similarly, there is no lineage restriction synencephalon, dorsal thalamus, and ventral thalamus. Pat- between the parencephalon and the more rostral forebrain terning of the diencephalon has been proposed to involve (secondary prosencephalon). Subdivision of the parencephalon subdivision of its anteroposterior axis into segments, neuro- into ventral and dorsal thalamus involves the formation of a meres or prosomeres (Bergquist and Kallen, 1954; Vaage, 1969; narrow intraparencephalic territory, the zona limitans intrathal- Figdor and Stern, 1993; Rubenstein et al., 1994; Redies et al., amica (zli). This is correlated with the acquisition of cell lineage 2000; Yoon et al., 2000). However, the number and sequence of restriction at both anterior and posterior borders of the zli, the diencephalic neuromeres, or even their existence, are uncer- appearance of boundary-specific properties, and Gbx2 and tain. We have examined the proposed subdivisions by morphol- Dlx2 expression in dorsal thalamic and ventral thalamic territo- ogy, gene expression, acquisition of boundary-specific pheno- ries, respectively. At stage 22, the synencephalon is divided into types, and cell lineage restriction. We find that at stage 16 in two domains, distinguished by differential gene expression and chick the diencephalon is divided into synencephalon and tissue morphology, but associated with neither a boundary parencephalon. The synencephalon exhibits neuromeric mor- phenotype nor cell lineage restriction. Our results suggest that phology, expresses Prox, and acquires neuromere boundary the diencephalon does not have an overt segmental pattern. properties at its interface with both the midbrain and the paren- cephalon. Although the mesencephalic/synencephalic bound- Key words: diencephalon; CNS; segmentation; neuromeres; ary restricts cell mixing, the synencephalic/parencephalic boundaries; compartments The most studied example of segmentation in the vertebrate CNS sialylated NCAM, peanut agglutinin-binding proteins, and vi- is the hindbrain, the anteroposterior axis of which is subdivided mentin (Lumsden and Keynes, 1989; Layer and Alber, 1990; into eight rhombomeres (Lumsden and Keynes, 1989; Cambron- Heyman et al., 1995). Some or all of these specializations may ero and Puelles, 2000). Rhombomeres are units of cell lineage reinforce the initial lineage restriction; some may also encourage restriction (Fraser et al., 1990), arranged in an alternating repeat the growth of axons and the formation of a precocious marginal pattern of odd and even character, that are thought to be of zone, a further feature of maturing inter-rhombomere bound- central importance in the acquisition of subregional identity aries (Lumsden and Keynes, 1989). (Lumsden and Keynes, 1989; Lumsden and Krumlauf, 1996). The Many attempts have been made to describe forebrain develop- establishment of lineage restriction at the interfaces between ment in the context of neuromery. On the basis of morphology rhombomeres, thereby containing cells within a developmental (Bergquist and Kallen, 1935; Coggeshall, 1964; Vaage, 1969; compartment, appears to be a function of immiscibility between Keyser, 1972) and gene expression (Bulfone et al., 1993; Ruben- odd and even cell populations (Wizenmann and Lumsden, 1997). stein et al., 1994), the diencephalon has been subdivided into The molecular basis of immiscibility has been ascribed to Eph/ three neuromeres (or prosomeres), corresponding with the syn- ephrin interaction at the odd/even interface (Mellitzer et al., encephalon (presumptive pretectum), posterior parencephalon 1999; Xu et al., 1999). Boundary cells, which specialize after the (presumptive dorsal thalamus), and anterior parencephalon (pre- formation of immiscibility interfaces, have characteristics that sumptive ventral thalamus). Figdor and Stern (1993) further distinguish them from cells within the rhombomere bodies: in- divided the synencephalon into posterior and anterior regions terkinetic nuclear migration is disrupted (Guthrie et al., 1991), and made the important claim that diencephalic neuromeres are, followed by an increase in extracellular space, expression of like rhombomeres, true neural segments, i.e., they are compart- chondroitin sulfate proteoglycan (CSPG), laminin, weakly poly- ments defined by cell lineage restriction. Alternating expression patterns of acetylcholinesterase and PNA binding suggested a Received Dec. 27, 2000; revised Feb. 26, 2001; accepted March 14, 2001. This work was supported by grants from the Wellcome Trust, the Medical two-segment repeat, like the rhombomeres (Figdor and Stern, Research Council, and the European Union. We thank E. Pollerberg for the gift of 1993). antibodies. Because it would be expected that the forebrain and hindbrain Correspondence should be addressed to Andrew Lumsden, MRC Centre for Developmental Neurobiology, King’s College London, London SE1 1UL, England. would share the same segmentation mechanism, we have at- E-mail: [email protected]. tempted to characterize putative diencephalic neuromeres ac- C. Larsen’s present address: Division of Mammalian Development, National Institute for Medical Research, The Ridgeway, Mill Hill, London, NW7 1AA, cording to criteria established for rhombomeres. However, we England. find that of the proposed interneuromeric boundaries in the L. Zeltser’s present address: Department of Genetics and Development, and diencephalon, only those bordering the zona limitans intrathal- Center for Neurobiology and Behavior, Columbia University, New York, New York 10032. amica (zli; a narrow stripe of cells that lies between the pro- Copyright © 2001 Society for Neuroscience 0270-6474/01/214699-13$15.00/0 spective dorsal and ventral thalami) and the mesencephalic/syn- 4700 J. Neurosci., July 1, 2001, 21(13):4699–4711 Larsen et al. • Diencephalic Boundaries and Compartments encephalic (m/s) boundary exhibit both lineage restriction and taken through the in situ hybridization and immunohistochemistry to boundary cell properties. Others, such as the synencephalic/ detect BrdU. Dextran labeling. With a tungsten needle, a small hole was cut through parencephalic (s/p) boundary, express boundary properties tran- the mesenchyme and epithelium either just above the eye on the right siently, but there is no lineage restriction either here or between side of the embryo (facing upward) or in the most anterior dorsal part of the diencephalon and the secondary prosencephalon [the anteri- the midbrain. This hole was large enough to allow a micropipette to pass ormost region of the neural tube that encompasses the preoptic through without touching any tissue. To label cells, a mixture of area, hypothalamus, and telencephalon (Puelles et al., 1987)]. rhodamine- and biotin-labeled dextrans was injected by iontophoresis. Injection was confirmed by using a fluorescence microscope. Embryos Finally, the intrasynencephalic boundary is not associated with were fixed after 48 hr survival and taken through in situ hybridization as either a boundary phenotype or cell lineage restriction. Our described above. To detect labeled cells after in situ hybridization, results therefore indicate that diencephalic patterning does not embryos were incubated overnight with a 1:250 concentration of PO- involve overt segmental subdivision. conjugated streptavidin and detected as for the immunohistochemistry protocol. MATERIALS AND METHODS Chick embryos. Fertilized eggs (Rhode Island Red) were incubated at RESULTS 37°C in 40–50% humidity, until the desired developmental stage was Subdivision of the diencephalon on the basis of reached. Embryos for in situ hybridization and immunohistochemistry morphology and Nissl staining were fixed in 4% paraformaldehyde in PBS for 12 hr. For in vivo manipulation, eggs were windowed, and the embryo was visualized by Neuromeric morphology was originally defined as external bulges sub-blastodermal injection of India ink. of neuroepithelium delineated by grooves, which appear on the Whole-mount immunohistochemistry was as described by Lumsden ventricular surface as troughs delineated by ridges (von Baer, and Keynes (1989) with modifications: for the neurofilament-specific antibody RMO-270 (Zymed, San Francisco, CA), embryos were dehy- 1828). We have used three techniques to assess morphological drated through ascending methanol and incubated overnight at Ϫ20°C. subdivision of the diencephalon into putative neuromeres: scan- The embryos were rehydrated and washed in PBS containing 1% Tween ning electron microscopy, Nissl staining, and immunohistochem- (PBT). For all other antibodies used, embryos were immersed in cryo- ical analysis of neuronal distribution. protection solution (PBS containing 1% Triton X-100, 5% goat serum, and 8% sucrose) and incubated twice at Ϫ20°C until just frozen, allowing The first morphological subdivision of the diencephalon is the embryos to thaw and reach room temperature after each incubation. apparent at Hamburger and Hamilton stage (HH) 16, when the Immunohistochemistry on sections was performed on both paraffin synencephalon adopts a typical neuromeric phenotype (Fig. 1A– and frozen sections (standard protocols).
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