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PubMed2006

Development of DARPP-32-positive parts of fetal pig ganglionic eminence and ventral mesencephalon in organotypic slice co-cultures.

Neurons from the fetal pig dopaminergic ventral mesencephalon (VM) and basal ganglia anlage (the ganglionic eminence) were co-cultured as organotypic slice cultures to study the development of the two interconnected brain areas. During a short developmental period (E35-E42), a groove separates the ganglionic eminence into a lateral and a medial part. This was used (a) to study the developmental expression of the striatal marker protein, dopamine and adenosine 3,5-monophosphate regulated phospho-protein (DARPP-32) in the two parts and (b) to compare innervations of the two parts by tyrosine hydroxylase (TH)-positive, dopaminergic fibers from co-cultured slices of the ventral mesencephalon. DARPP-32 expression was more extensive and dense in cultures of the lateral part of the striatal anlage than the medial part. The DARPP-32-positive areas moreover overlapped with areas rich in acetylcholine esterase (AChE) and were the preferred target areas for TH-positive fibers from the co-cultured VM.

Animals↗

PubMed1994

The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence.

In order to determine whether the lateral ganglionic eminence (LGE) of the fetal telencephalon is the primary source of striatal precursors in striatal transplants and tissue cultures, cells derived exclusively from the LGE of fetal rat brains were transplanted into the quinolinic-acid-lesioned striatum of adult rats. After 2-3 months they produced grafts that were almost entirely AChE-positive as well as DARPP-32-, TH-, and calbindin-immunoreactive. The grafts were integrated into the host striatum so that host corticofugal fiber tracts interdigitated with graft tissues similar to the way they penetrate the gray matter of the normal striatum. Fast Blue dye injected into the ipsilateral globus pallidus of LGE grafted produced retrogradely labeled neurons within the grafts, but Fluorogold dye injected into the ipsilateral substantia nigra did not. In a separate experiment using DARPP-32-immunohistochemstry as a striatal marker, fetal (E16) and neonatal (P2) rat brains showed DARPP-32 immunoreactivity in the LGE but not in the adjacent medial ganglionic eminence (MGE). In summary, both fetal LGE cells and LGE grafts express specific striatal markers, and LGE grafts integrate into the host striatum and innervate the major striatal efferent target within the host brain. These data suggest that the LGE is the origin of cells committed to striatal phenotypes in the developing brain.

Acetylcholinesterase↗

PubMed2005

Ventralized dorsal telencephalic progenitors in Pax6 mutant mice generate GABA interneurons of a lateral ganglionic eminence fate.

The transcription factor Pax6 is expressed by progenitors in the ventricular zone (VZ) of dorsal telencephalon (dTel), which generate all cortical glutamatergic neurons, but not by progenitors in the medial ganglionic eminence (MGE), which generate cortical GABAergic interneurons (GABA INs), or the lateral ganglionic eminence (LGE), which generate GABA INs that normally migrate to the olfactory bulb. We show that perinatally, Pax6(sey/sey) mice, which lack functional Pax6 protein, have large subpial ectopias in dTel and ventral telencephalon connected by cell streams arising from an aberrant paraventricular ectopia found throughout dTel. The subpial and paraventricular ectopias and connecting cell streams are comprised of postmitotic neurons expressing markers for GABA INs characteristic of a LGE fate. Marker analyses show that dTel VZ progenitors in Pax6 mutants are progressively ventralized, acquiring expression of regulatory genes normally limited to GE progenitors; by midneurogenesis, the entire dTel VZ exhibits ventralization. This ventralization of the dTel VZ is paralleled by the expression of markers for GABA INs superficial to it, suggesting that it ectopically produces GABA INs, leading to their ectopias and a thinner cortical plate due to diminished production of glutamatergic neurons. Genetic lineage tracing demonstrates that the GABA INs comprising the ectopias are from a cortical Emx1 lineage generated in the dTel VZ, definitively showing that dTel progenitors and progeny acquire a ventral, GE, fate in Pax6 mutants. Thus, Pax6 delimits the appropriate proliferative zone for GABA INs and regulates their numbers and distributions by repressing the ventral fates of dTel progenitors and progeny.

Animals↗

PubMed1996

The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons.

In the nervous system of many species, growing axons associate transiently with cellular groupings along their path. Whether this mechanism applies to the development of corticothalamic and thalamocortical projections is unknown. Using carbocyanine dyes, we studied the early growth of both corticofugal and thalamocortical fibers in hamster embryos. At embryonic day 11.5 (E11.5), corticofugal fibers invade the lateral ganglionic eminence (LGE), and thalamocortical fibers invade the medial ganglionic eminence (MGE). At this age, both sets of fibers are not yet in contact with each other. At the same time, neurons in each subdivision of the GE grow toward the cortex and thalamus. During the next 24 hr, corticofugal and thalamocortical fibers remain within the confines of the GE, where they course at different radial levels and bear large and complex growth cones. In the LGE, corticofugal fibers are often found in close association with cells that are likely to be neuronal. Starting on E13.5, both early projections from the GE decrease, and corticothalamic and thalamocortical fibers invade their definitive target regions. To test whether the GE specifically orients the growth and trajectories of cortical fibers even in the absence of the reciprocal thalamic projection, we cocultured explants of cortex and GE from either hamster or mouse embryos. These experiments showed that the GE, but not other tested brain regions, is able specifically to orient the growth of cortical axons. We therefore suggest that the GE may be an intermediate target in the pathfinding of axons between the cortex and the thalamus.

Animals↗

PubMed2003

Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis.

The lateral ganglionic eminence (LGE) is known to give rise to striatal projection neurons as well as interneurons, which migrate in the rostral migratory stream (RMS) to populate the granule cell and glomerular layers of the olfactory bulb. Because all of these neuronal subtypes express Distalless-related (DLX) homeobox proteins during their differentiation, we set out to further characterize progenitors in the Dlx-positive domain of the LGE. Previous studies have shown that the LIM homeobox protein Islet1 (ISL1) marks the LGE subventricular zone (SVZ) and differentiating striatal projection neurons. However, ISL1 is not expressed in neurons of the developing olfactory bulb or the RMS. We show here that the dorsal-most portion of the Dlx-expressing region of the LGE SVZ lacks ISL1 cells. This dorsal domain, however, contains cells that express the ETS transcription factor Er81, which is also expressed in granule and periglomerular cells of the developing and adult olfactory bulb. Moreover, the adult SVZ and RMS contain numerous Er81-positive cells. Fate-mapping studies using Dlx5/6-cre transgenic mice demonstrate that Er81-positive cells in the granule cell and glomerular layers of the olfactory bulb derive from the Dlx-expressing SVZ region. These findings suggest that the LGE SVZ contains two distinct progenitor populations: a DLX(+);ISL1(+) population representing striatal progenitors and a DLX(+);Er81(+) population comprising olfactory bulb interneuron progenitors. In support of this, mice mutant for the homeobox genes Gsh2 and Gsh1/2, which show olfactory bulb defects, exhibit dramatically reduced numbers of Er81-positive cells in the LGE SVZ as well as in the olfactory bulb mantle.

Animals↗

PubMed2000

Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons.

GABAergic interneurons have major roles in hippocampal function and dysfunction. Here we provide evidence that, in mice, virtually all of these cells originate from progenitors in the basal telencephalon. Immature interneurons tangentially migrate from the basal telencephalon through the neocortex to take up their final positions in the hippocampus. Disrupting differentiation in the embryonic basal telencephalon (lateral and medial ganglionic eminences) through loss of Dlx1/2 homeobox function blocks the migration of virtually all GABAergic interneurons to the hippocampus. On the other hand, disrupting specification of the medial ganglionic eminence through loss of Nkx2.1 homeobox function depletes the hippocampus of a distinct subset of hippocampal interneurons. Loss of hippocampal interneurons does not appear to have major effects on the early development of hippocampal projection neurons nor on the pathfinding of afferrent tracts.

Animals↗

PubMed1996

DARPP-32-rich zones in grafts of lateral ganglionic eminence govern the extent of functional recovery in skilled paw reaching in an animal model of Huntington's disease.

Grafts of striatal tissue comprise two different types of tissue: regions with (P-zones) and without (NP-zones) neurons that express markers characteristic of the striatum, such as dopamine- and cyclic AMP-regulated phosphoprotein with a mol. wt of 32,000 (DARPP-32). It remains unclear whether P-zones alone play a crucial role in functional effects of striatal grafts in an animal model of Huntington's disease. The present study has been performed to determine: (i) the yield of DARPP-32-positive neurons in grafts of lateral ganglionic eminence; (ii) whether treatment of graft tissue with the spin-trapping agent alpha-phenyl-tert-butyl nitrone enhances the survival of implanted DARPP-32-positive neurons; and (iii) the relationship between the number of DARPP-32-positive neurons in the grafts and functional effects of the grafts on paw-reaching ability in rats with unilateral quinolinic acid lesions of the striatum. Dissociated tissue derived from the lateral ganglionic eminence of rat embryos (embryonic day 14), with or without addition of alpha-phenyl-tert-butyl nitrone (3 mM), was implanted into the quinolinic acid-lesioned striatum. Compared to unlesioned normal animals, rats with striatal lesions showed substantial impairment in paw-reaching ability, particularly on the side contralateral to the lesion, as judged from the number of pellets retrieved by each paw. Intrastriatal grafts gave rise to a significant improvement in paw-reaching ability. The mean total number of surviving DARPP-32-positive cells in grafts without alpha-phenyl-tert-butyl nitrone treatment was estimated at 115 x 10(3), which did not significantly differ from that in alpha-phenyl-tert-butyl nitrone-treated grafts. The paw-reaching scores were significantly correlated with the volumes of P-zones and the number of DARPP-32-positive neurons, but with neither the volumes of NP-zones nor the total graft volume. The results suggest that P-zones in striatal grafts mediate graft-derived functional recovery in a complex task such as skilled forelimb use. Although the antioxidant treatment with alpha-phenyl-tert-butyl nitrone failed to promote graft survival, the positive correlation between the yield of DARPP-32-positive cells in the graft and the extent of the functional recovery highly warrants further attempts to increase the yield of the striatal component in the graft.

Acetylcholinesterase↗

PubMed2005

Early regionalisation of the neocortex and the medial ganglionic eminence.

The two major functional classes of neurons that build the cerebral cortex are generated in two distinct parts of the telencephalon. Excitatory long distance projecting neurons are produced dorsally in the pallium, whereas local inhibitory interneurons are mainly produced in the medial ridge of the ventral telencephalon. These two parts of the telencephalon are molecularly regionalized from early embryonic stages, but cellular indices of regionalisation are observed only at later stages of development. We have looked for cellular indices of regionalisation in the cortical anlage at early embryonic stages, when the first efferent cortical neurons are generated. Similarly, we have looked for functional regionalisation of the medial ganglionic eminence at the same stages, when the future cortical interneurones are generated. Here, we summarize data showing that two regions in the mouse cortex embryo, the lateral and dorsal cortex, differ strongly in their early neurogenesis. Moreover, the two domains differ in their capacity to produce GABAergic neurons in vitro; this capacity is only observed in the dorsal cortex. The differentiation of the two domains appears to be independent of the laterorostral to mediocaudal gradient of maturation of the cortex. In the basal telencephalon too, the capacity to differentiate GABAergic neurons is not uniformly distributed across the medial ganglionic eminence. The neurogenesis of future cortical interneurons is seen to be highly active in a small area located in the rostral MGE, at mid dorso-ventral level.

Animals↗

PubMed2003

Permissive corridor and diffusible gradients direct medial ganglionic eminence cell migration to the neocortex.

Young neurons born in the medial ganglionic eminence (MGE) migrate a long distance dorsally, giving rise to several types of interneurons in neocortex. The mechanisms that facilitate selective dorsal dispersion of MGE cells while restricting their movement ventrally into neighboring regions are not known. Using microtransplantation into fetal brain slices and onto dissociated substrate cells on floating filters (spot assay), we demonstrate that ventral forebrain regions neighboring the MGE are nonpermissive for MGE cell migration, whereas the dorsal regions leading to the neocortex are increasingly permissive. Spot assay experiments using filters with different pore sizes indicate that the permissive factors are not diffusible. We also show that MGE cells respond to chemoattractive and inhibitory factors diffusing from the neocortex and ventromedial forebrain, respectively. We propose that the final extent and regional specificity of MGE cell dispersion is largely dictated by contact guidance through a selectively permissive environment, flanked by nonpermissive tissues. In addition, we propose that chemotactic guidance cues superimposed over the permissive corridor facilitate efficient dorsal migration of MGE cells.

Animals↗

PubMed1976

A pilot study of cell production by the ganglionic eminences of the developing mouse brain.

Cell production in the medial and lateral ganglionic eminences in pre- and post-natal mouse brains was studied by recording the number, location and plane of cleavage of mitotic figures. The site of maximum cell production shifted progressively from the ependymal layer to an adjacent sub-ependymal proliferative compartment. In the latter, mitosis occurred without the nuclei participating in the migratory movement to the ventricular surface which is characteristic of the nuclei of the ependymal compartment. The sub-ependymal compartment persisted vestigially into post-natal life as the well known sub-ependymal layer.

Animals↗

PubMed1999

Long-term survival of fetal porcine lateral ganglionic eminence cells in the hippocampus of rats.

Embryonic porcine brain tissue from the lateral ganglionic eminence was transplanted into the adult rat hippocampus to determine whether fetal striatal cells could survive, differentiate, and integrate in a heterotopic site. The hippocampus, a common site of epileptic seizure activity, was chosen to determine if fetal striatal cells could supply inhibitory GABAergic neurons that may serve to block seizures. Cells were either implanted with a single deposit using a standard metal cannula or by five smaller disseminated deposits with a glass micropipette. At 20-24 weeks, animals immunosuppressed with cyclosporin showed long-term survival of porcine cells in the adult hippocampus. Analysis by immunohistochemistry and in situ hybridization showed that the grafts contained glial and neuronal cell types, including GABAergic neurons within graft core and networks of porcine neuronal fibers extending from the graft into the host parenchyma. In addition, a marker of porcine presynaptic terminals, synaptobrevin, was abundant within the grafts and was found associated with hippocampal structures and cell layers suggesting functional integration of grafted cells within the host. The survival of xenografts in the hippocampus and potential integration of inhibitory components provides evidence that these grafts may serve as an internal negative feedback mechanism to quench epileptiform activity.

Animals↗

PubMed2003

Neuronal and glial differentiation within expanded glial cultures derived from the lateral and medial ganglionic eminences.

Attached glial-like cell cultures were established from the lateral and medial ganglionic eminences (LGE and MGE) and from the neocortex (Cx) of E13.5 mouse embryos, and expanded over four to five passages under epidermal growth factor (EGF) stimulation. Following removal of EGF and serum, we analysed the generation of neurons and glial cells within the cultures. Significant numbers of betaIII-tubulin-positive neurons were generated in both the LGE (about 7% of total cell numbers) and the MGE (around 2%). However, only few betaIII-tubulin-positive cells with neuronal morphologies were detected in the differentiated Cx cultures. The newly formed neurons were to a large extent GABAergic, and many of the MGE-derived, but not the LGE-derived, cells expressed the MGE-marker NKX2.1. Most cells in all cultures still appeared astroglial-like, expressing glial fibrillary acidic protein (GFAP), but in addition, CNPase-positive cells with oligodendroglial morphologies were present in the MGE (0.68%), and, to a lesser extent (0.2%), in the LGE cultures. The present results demonstrate that cells of expanded glial cultures from both the LGE and MGE can give rise to significant and, to a certain extent, region-specific neuronal and glial cell types under differentiating conditions.

2',3'-Cyclic-Nucleotide Phosphodiesterases↗

PubMed2005

The caudal migratory stream: a novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain.

The migratory paths of interneurons derived from the ganglionic eminence (GE), and particularly its caudal portion (CGE), remain essentially unknown. To clarify the three-dimensional migration profile of interneurons derived from each part of the GE, we developed a technique involving focal electroporation into a small, defined portion of the telencephalic hemisphere. While the medial GE cells migrated laterally and spread widely throughout the cortex, the majority of the CGE cells migrated caudally toward the caudal-most end of the telencephalon. Time-lapse imaging and an in vivo immunohistochemical study confirmed the existence of a migratory stream depicted by a population of CGE cells directed caudally that eventually reached the hippocampus. Transplantation experiments suggested that the caudal direction of migration of the CGE cells was intrinsically determined as early as embryonic day 13.5. The caudal migratory stream is a novel migratory path for a population of CGE-derived interneurons passing from the subpallium to the hippocampus.

Animals↗

PubMed2004

Expression patterns of PSA-NCAM in the human ganglionic eminence and its vicinity: role of PSA-NCAM in neuronal migration and axonal growth?

The ganglionic eminence (GE) is a transient but conspicuous structure of the developing forebrain which not only gives rise to a large number of precursor neurons and glial cells for various structures of the forebrain, but in addition serves as an intermediate target for growing axons to the cerebral cortex. To investigate the roles of the highly polysialylated isoform of the neural cell adhesion molecule (PSA-NCAM) in cell migration and axonal growth within the GE and its neighbouring structures, the spatio-temporal expression pattern of PSA-NCAM was examined in human fetal forebrains between 14 and 36 weeks of gestation with a specific immunohistochemical method. Scattered PSA-NCAM-positive cells were found in the centre but more frequently in the marginal zone of the GE. Intensely labelled cells were also identified in the gangliothalamic body, basolateral nuclei of the amygdala and the subventricular and intermediate zone adjacent to the GE. This cellular immunoreactivity started to appear in various structures during the period from 14 to 19 weeks and gradually diminished after 25-28 weeks. Strong immunoreactivity was also detected in fibres running from the intermediate zone of the neocortex to the internal capsule from 16 weeks onwards, and after 24 weeks, the immunoreactivity was gradually decreased. In the vicinity of the GE, between 16 and 22 weeks, short fibre bundles were observed to leave the longitudinally oriented axons of the internal capsule to reach the marginal zone of the GE. Our results suggest a close relationship between PSA-NCAM expression and neuronal migration (over short distances) and transitory axonal projections (target recognition and axonal fasciculation) in the region of the GE.

Axons↗

PubMed2000

Long-term, EGF-stimulated cultures of attached GFAP-positive cells derived from the embryonic mouse lateral ganglionic eminence: in vitro and transplantation studies.

Long-term attached cultures, prepared from mouse embryonic days 15-17 lateral ganglionic eminence, were grown in a medium including epidermal growth factor and serum, and the survival, differentiation, and migration of cells from either early or late passages were analyzed following transplantation. The cultured cells had the morphology of type I astroglial cells, with the vast majority of the cells immunoreactive for glial fibrillary acidic protein (around 90%), the intermediate filament marker nestin, and also the mouse-specific neural markers M2 and M6. The cultures were kept over 25 passages (7 months). During the first 8 passages, the growth rate gradually declined, but it increased again after passage 9 and thereafter stabilized at values similar to those observed during the initial culture period. After passages 4-6 and 18, cell suspensions were implanted cross-species into the intact or lesioned striatum of adult (passages 4-5 only) or intact striatum of neonatal rats (passages 4-6 or 18). Both early and late passage cells formed M2 (and M6)-positive transplants. In the neonatal recipients, widespread migration was seen from the needle tract throughout most of the striatum, along the internal capsule, and into the globus pallidus. In the adult striatum, the cells remained mostly around the injection tract, or within 0.4-0.6 mm from the graft core. These long-term attached cultures are interesting to compare to nonattached neurosphere cultures, and might also offer a means of propagating relatively pure populations of astroglia-like cells for basic transplantation studies or for use in experimental trials with ex vivo gene transfer.

Animals↗

PubMed2001

The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system.

Cortical nonpyramidal cells, the GABA-containing interneurons, originate mostly in the medial ganglionic eminence of the ventral telencephalon and follow tangential migratory routes to reach the dorsal telencephalon. Although several genes that play a role in this migration have been identified, the underlying cellular and molecular cues are not fully understood. We provide evidence that the neural cell adhesion molecule TAG-1 mediates the migration of cortical interneurons. We show that the migration of these neurons occurs along the TAG-1-expressing axons of the developing corticofugal system. The spatial and temporal pattern of expression of TAG-1 on corticofugal fibers coincides with the order of appearance of GABAergic cells in the developing cortex. Blocking the function of TAG-1, but not of L1, another adhesion molecule and binding partner of TAG-1, results in a marked reduction of GABAergic neurons in the cortex. These observations reveal a mechanism by which the adhesion molecule TAG-1, known to be involved in axonal pathfinding, also takes part in neuronal migration.

Animals↗

PubMed2002

Ganglionic eminence of the human fetal brain--new vistas.

This review deals with recent findings concerning the complex functions of the ganglionic eminence (GE), which represents a conspicuous domain of the telencephalic proliferative zone and persists nearly throughout fetal life. The GE not only contains precursor neurons of the basal ganglia, it also contributes significantly to the population of interneurons in the cerebral cortex and to a population of thalamic neurons. The latter migrate through a distinct transient structure, the gangliothalamic body (GTB). The GE also represents an intermediate target for growing thalamic axons (on their way to the cerebral cortex) and cortical axons (on their way to the thalamus). In developmental neuropathology the GE plays an important role in prematurely born infants. The pathogenesis of GE bleedings is discussed with regard to the abundant expression of interleukin-6 (IL-6) receptors on GE cells. The consequences of such bleedings are discussed in view of cellular responses, such as the induction of leukemia inhibitory factor (LIF) expression in GE cells after hemorrhage.

Cell Movement↗

PubMed2003

The differentiation potential of precursor cells from the mouse lateral ganglionic eminence is restricted by in vitro expansion.

We have investigated whether the differentiation potential of attached cultures derived from the mouse lateral ganglionic eminence (LGE) is influenced by in vitro expansion. Primary neuronal cultures derived from the LGE give rise to neurons expressing the striatal projection neuron markers Islet1 (ISL1) and dopamine and cAMP-regulated phosphoprotein of 32 kilodaltons (DARPP-32) as well as the olfactory bulb interneuron marker Er81. Our previous results showed that after expansion in vitro, LGE precursor cells can be induced to differentiate into neurons which exhibit molecular characteristics of the LGE, such as the homeobox transcription factors DLX and MEIS2. We show here that while attached LGE cultures maintain Er81 expression through five passages, they lose the ability to generate ISL1- or dopamine and cAMP-regulated phosphoprotein of 32 kilodaltons-expressing neurons already after the first passage. This indicates that the expansion of LGE precursor cells restricts their differentiation potential in vitro. Interestingly, the undifferentiated LGE cultures retain the expression of both the Isl1 and Er81 genes, suggesting that precursor cells for both striatal projection neurons and olfactory bulb interneurons are present in these cultures. Thus the restriction in differentiation potential of the expanded LGE cultures likely reflects deficiencies in the differentiation conditions used.

Aging↗