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Clones in the Chick Diencephalon Contain Multiple Cell Types and Siblings Are Widely Dispersed

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Clones in the Chick Diencephalon Contain Multiple Cell Types and Siblings Are Widely Dispersed Development 122, 65-78 (1996) 65 Printed in Great Britain © The Company of Biologists Limited 1996 DEV8292 Clones in the chick diencephalon contain multiple cell types and siblings are widely dispersed Jeffrey A. Golden1,2 and Constance L. Cepko1,3 1Department of Genetics, Harvard Medical School, 2Department of Pathology, Brigham and Women’s Hospital, and 3Howard Hughes Medical Institute, 200 Longwood Avenue, Boston, MA 02115, USA SUMMARY The thalamus, hypothalamus and epithalamus of the ver- clones dispersed in all directions, resulting in sibling cells tebrate central nervous system are derived from the populating multiple nuclei within the diencephalon. In embryonic diencephalon. These regions of the nervous addition, several distinctive patterns of dispersion were system function as major relays between the telencephalon observed. These included clones with siblings distributed and more caudal regions of the brain. Early in develop- bilaterally across the third ventricle, clones that originated ment, the diencephalon morphologically comprises distinct in the lateral ventricle, clones that crossed neuromeric units known as neuromeres or prosomeres. As development boundaries, and clones that crossed major boundaries of proceeds, multiple nuclei, the functional and anatomical the developing nervous system, such as the diencephalon units of the diencephalon, derive from the neuromeres. It and mesencephalon. These findings demonstrate that prog- was of interest to determine whether progenitors in the enitor cells in the diencephalon are multipotent and that diencephalon give rise to daughters that cross nuclear or their daughters can become widely dispersed. neuromeric boundaries. To this end, a highly complex retroviral library was used to infect diencephalic progeni- tors. Retrovirally marked clones were found to contain Key words: cell lineage, central nervous system, diencephalon, neurons, glia and occasionally radial glia. The majority of thalamus, chick, thalamus, hypothalamus INTRODUCTION of the diencephalon resembles the more caudal mesencephalon (midbrain) and rhombencephalon (hindbrain), which are One of the hallmarks of the adult nervous system is the parceled into discrete nuclei with mostly discrete projections. exquisite complexity of its cell types and synaptic connections. How the intermediate structure of the diencephalon develops The mechanisms that generate complexity during development is not clear. The development of some of the more rostral and remain largely unknown. Early in development, the neural tube caudal regions of the brain have been relatively well described is thought to be parceled into unique units or segments such that we can now appreciate that these areas follow (Lumsden, 1990; Puelles and Rubenstein, 1993; Rubenstein et different rules in key aspects of their development. al., 1994; Rubenstein and Puelles, 1994). Distinct morphologi- The rhombencephalon is transiently parceled into 8 mor- cal units first appear shortly before neural tube closure when phologically identifiable units known as rhombomeres. The multiple vesicular outpouchings develop rostrally. The primary neurons in each rhombomere comprise groups of nuclei, each vesicles are termed the prosencephalon, the mesencephalon with defined functions and a stereotypical pattern of axonal and the rhombencephalon. The prosencephalon gives rise to projections (Lumsden and Keynes, 1989; Keynes and the telencephalon (cerebral hemispheres) and the dien- Lumsden, 1990; Lumsden, 1990). A molecular basis for the cephalon. The diencephalon is the embryonic precursor to the morphological and functional specification of rhombomeres hypothalamus, thalamus and epithalamus, and is anatomically has been established through studies of the expression and mis- situated between the cerebral hemispheres and more caudal expression of Hox genes and other transcription factors areas of the brain. The diencephalon appears to be conserved (Guthrie and Lumsden, 1991, 1992; Hunt et al., 1991; Guthrie structurally and functionally throughout evolution, although et al., 1992). Lineage analysis conducted in the hindbrain of there is some debate about whether the organization within the chicks has shown that once the boundaries of the rhombomeres diencephalon, and the thalamus in particular, is similar across are established, the majority of clones appear to be restricted species (Kappers et al., 1960; Jones, 1985). The embryologi- to a single rhombomere (Fraser et al., 1990; Birgbauer and cal origin of the diencephalon appears to be conserved in Fraser, 1994) during the next 48 hours of development. Clones disparate species (Kappers et al., 1960). also appear restricted in cell fate in that most clones comprise While functional aspects of the diencephalon appear to siblings that adopt the same or a related neuronal cell fate mimic the rostral telencephalon, the anatomical organization (Lumsden et al., 1994). 66 J. A. Golden and C. L. Cepko The telencephalon, the most rostral part of the central neuromeric units (Bulfone et al., 1993a,b; Rubenstein et al., nervous system (CNS), is not separated into morphologically 1994; Rubenstein and Puelles, 1994), similar to the correlation defined, repeated units. Rather, the cerebral cortex, the largest noted in the hindbrain. Short-term lineal relationships in the component of the telencephalon, is organized into a diffuse diencephalon have been analyzed using the method of single laminated sheet of cells. Although the cortex can be parceled cell microinjection of a fluorescent dye (Figdor and Stern, into functional domains, there is no discrete nuclear organiz- 1993). The results indicated that the morphological neuromeres ation as is found in the hindbrain and diencephalon. Studies of the diencephalon are akin to the hindbrain rhombomeres in investigating the expression pattern of a variety of genes, that clones were restricted to a single neuromere up to 48 hours mostly transcription factors, have uncovered several genes after injection, the latest time point analyzed. However, this with nested (Simeone et al., 1992; Bulfone et al., 1993a,b) or technique precludes analysis of the final patterns of clonal dis- lamina-specific (Frantz et al., 1994a,b; Leifer et al., 1994) persion or the mature cell types within any one clone. patterns of expression. However, genes investigated thus far Chick/quail chimera studies have also been performed in the are generally not expressed within morphologically or physio- diencephalon (Martinez and Alvarado-Mallart, 1989). In these logically defined areas. Lineage analysis in the telencephalon studies, quail mesencephalon was transplanted into chick dien- has demonstrated that siblings spread over great distances to cephalon, and thus the potential of diencephalic progenitors give rise to neurons in functionally and anatomically unrelated was not tested. Nonetheless, these studies indicated that mes- parts of the cerebral cortex (Walsh and Cepko, 1992, 1993; encephalic progenitors dispersed to populate several, but not Reid et al., 1995). Lineage analysis in the telencephalon has all, nuclei in the diencephalon. One interesting pattern of shown that individual progenitor cells are capable of generat- spread for the mesencephalic progenitors in these studies was ing neurons and glia (Price and Thurlow, 1988; Walsh and that they selectively populated primary visual nuclei, suggest- Cepko, 1992; Levison et al., 1993; Reid et al., 1995). In the ing a relationship with the tectum, the normal derivative of the retina (an outgrowth of the diencephalon) and the chick tectum mesencephalon. (a derivative of the mesencephalon), lineage analysis has also Using a complex retroviral library comprising DNA tags as shown that neurons and glia arise from a common progenitor lineage markers (Golden et al., 1995), we have evaluated 275 cell (Turner and Cepko, 1987; Galileo et al., 1990; Turner et clones in the chick diencephalon. This technique allows al., 1990; Gray and Sanes, 1992; Fekete et al., 1995). analysis of clones in the mature diencephalon, after clonal dis- The diencephalon is organized into individual nuclei (col- persion is complete. We found that sibling cells can spread lections of neurons with a specific projection or defined set of extensively within the diencephalon, sometimes occupying projections) with some groups of nuclei having similar func- nuclei derived from more than one neuromere. Dispersion tional properties and other neighboring nuclei having distinct occasionally led to cells being located in both the diencephalon functions. Functionally, however, the diencephalon and, par- and the mesencephalon. Furthermore, siblings were found on ticularly, the thalamus closely resemble the telencephalon both the left and right sides of the third ventricle in approxi- (cerebral cortex and basal ganglia). The thalamus functions as mately 16% of the clones. We also found that progenitors of the major integration and projection region to the cerebral diencephalic cells were located in the ventricular zone of the cortex from more caudal structures, including the spinal cord, third ventricle, as well as in the ventricular zone of the lateral cerebellum, hindbrain and midbrain (Jones, 1985). The ventricle. Clones frequently contained neurons, glia and radial neurons of the thalamic nuclei project to different cortical areas glia, supporting the existence of multipotent progenitor cells. with many thalamic nuclei projecting to overlapping cortical regions. Furthermore, the thalamocortical projections to
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