An Excitatory GABAergic Plexus in Developing Neocortical Layer 1

Dammerman, Ryan; Flint, Alexander C.; Noctor, Stephen C.; Kriegstein, Arnold R.

doi:10.1152/jn.2000.84.1.428

Cited by 66 publications

(52 citation statements)

References 42 publications

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“…At midgestation, MZ pioneer neurons receive functional GABA A -mediated synaptic inputs. These inputs most likely originate from GABAergic fibers located in the MZ (6,40) although their exact origin cannot be elucidated unequivocally. These GABA Amediated events may have a depolarizing action as previously suggested during early cortical development (41,42).…”

Section: Discussionmentioning

confidence: 99%

Subpallial origin of a population of projecting pioneer neurons during corticogenesis

Morante

Carleton

Ortino

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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T wo germinative zones of the telencephalon, the dorsal (pallial) and the ventral (subpallial) ventricular zones (VZ), provide new neurons to the cerebral cortex. Postmitotic cells from the dorsal VZ differentiate into excitatory projection neurons after a radial migration whereas the ventral part of the VZ, including the lateral (LGE), medial (MGE), and caudal ganglionic eminences, generates neurons of the basal ganglia and cortical interneurons (1-7). The cortical neurons, born early to form the preplate, are thought to function as a scaffold for the assembly of the cortical architecture (8-12). Other cortical neurons, born later, migrate radially and insert themselves into the preplate to generate the cortical plate (CP), which splits the preplate into the marginal zone (MZ) and the subplate (SP) (8, 11).Cajal-Retzius cells, which reside in the preplate and thereafter in the MZ, are considered to be the earliest neurons to differentiate in the developing neocortex (8). These cells secrete reelin (13-19), an extracellular matrix glycoprotein that is crucial for cortical lamination (20,21). Pioneer neurons are also preplatederived; they guide thalamocortical afferent axons into the cortex and cortical efferent axons to their subcortical targets (10, 11). Recently, we described a population of pioneer neurons in the MZ (17,18,22,23), but their origins, their molecular properties, and their functions remained unexplored (12,24). We here characterize the MZ pioneer neurons by combining cell tracers and cell-specific markers with patch-clamp recordings. We found that the adhesion molecules TAG-1 and L1 are reliable markers of such neurons. We show that MZ pioneer neurons migrate tangentially to the MZ from subpallial sources. We demonstrate that such a migration is reelin-dependent and, in addition, that reelin controls the arrival of MGE-derived interneurons to the CP during early corticogenesis. Materials and MethodsOrganotypic Slices. Brains were obtained from embryos of pregnant OF1 mice at embryonic day 14 (E14) (Iffa Credo; n ϭ 64; date of plug ϭ E0). All animals used in this study were maintained and treated according to protocols approved by the authors' institutions. Dams were killed by cervical dislocation under Isof lurane anesthesia (Belamont, Neuilly-sur-Seine, France). The uterus and embryos were removed and rapidly isolated in cold oxygenated (5% CO 2 and 95% O 2 ) artificial corticospinal fluid (in mM): 124 NaCl, 3 KCl, 1.3 MgSO 4 , 26 NaHCO 3 , 1.25 NaH 2 PO 4 , 10 glucose, and 2 CaCl 2 . Brains were embedded in 4% agar and coronally sliced (300 m) with a vibrating microtome (VT-1000, Leica, Argenteuil, France). Slices were placed onto Millicell-CM membranes (Millipore, Bedford, MA) in 35-mm Petri dishes containing 1 ml of the following medium (Life Technologies, Cergy Pontoise, France): 50% basal medium with Eagle's salts, 25% horse normal serum, 25% Hanks' balanced salt solution, 4.5 mg͞ml D-glucose, and 0.1 mM L-glutamine (25). The medium had been heated previously at 56°C for 30 min to inactiva...

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Section: Discussionmentioning

confidence: 99%

Subpallial origin of a population of projecting pioneer neurons during corticogenesis

Morante

Carleton

Ortino

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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“…GABA is known to have a depolarizing effect on neural progenitor cells and immature neurons, both during developmental and adult neurogenesis (LoTurco et al, 1995;Dammerman et al, 2000;Ge et al, 2006). A subpopulation of nestin + precursor cells in the DG express functional GABA A receptors (Tozuka et al, 2005;Wang et al, 2005).…”

Section: Gabamentioning

confidence: 99%

Neurotransmitter-mediated control of neurogenesis in the adult vertebrate brain

et al. 2013

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SummaryIt was long thought that no new neurons are added to the adult brain. Similarly, neurotransmitter signaling was primarily associated with communication between differentiated neurons. Both of these ideas have been challenged, and a crosstalk between neurogenesis and neurotransmitter signaling is beginning to emerge. In this Review, we discuss neurotransmitter signaling as it functions at the intersection of stem cell research and regenerative medicine, exploring how it may regulate the formation of new functional neurons and outlining interactions with other signaling pathways. We consider evolutionary and cross-species comparative aspects, and integrate available results in the context of normal physiological versus pathological conditions. We also discuss the potential role of neurotransmitters in brain size regulation and implications for cell replacement therapies. Key words: Adult neurogenesis, Homeostasis, Neural stem cell, Neurotransmitter, Regeneration IntroductionIn the brain, signaling via neurotransmitters, small molecules released by neurons to communicate with other cells, has primarily been associated with the function rather than with the formation of neurons. However, several reports have identified roles for neurotransmitters in cell fate determination in a wide range of species both within and outside the central nervous system (CNS). A thorough discussion on the evolutionary origin of neurotransmitter signaling is outside the scope of this Review, but it is important to note that both neurotransmitters and their receptors (see Table 1) are present and functionally important in organisms without a nervous system. For example, γ-aminobutyric acid (GABA), glutamate and nitric oxide (NO) have all been detected in sponges and shown to regulate cell behavior (Ellwanger et al., 2007;Elliott and Leys, 2010). A recent transcriptome profiling of the sponge A. queenslandica revealed the expression of wide repertoire of components active in synapses found in the vertebrate nervous systems (Conaco et al., 2012). In the social amoeba Dictysotelium, disruption of a glutamate receptor by homologous recombination reveals a role for glutamate signaling in the suppression of cell division (Taniura et al., 2006), while GABA induces terminal differentiation of spores through a GABA B receptor (Anjard and Loomis, 2006). GABA and glutamate appear to play opposing roles in spore induction (Fountain, 2010) in Dictyostelium, indicating that the apparent antagonistic relationship between glutamate and GABA signaling was established prior to the evolution of synaptic communication in the CNS.Furthermore, neurotransmitters control cell proliferation during development long before the onset of neurogenesis in mammals, as exemplified by GABA signaling in the early embryo (Andäng et al., 2008). Once developmental neurogenesis is initiated, neurotransmitter signaling has an impact on several aspects of neurogenesis, including proliferation, migration and differentiation in various locations in the CNS, such as the tele...

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“…Whereas in the adult brain GABA A receptor activation has been related to the mediation of synaptic inhibition, in immature neurons this causes marked membrane depolarization that can induce action potential discharge (Ben-Ari et al, 1989;Owens et al, 1996Owens et al, , 1999Dammerman et al, 2000;Gao and van den Pol, 2001). The relatively higher intracellular chloride concentration is considered responsible for the observed response (Ben-Ari et al, 1989;Chen et al, 1996;Rohrbough and Spitzer, 1996).…”

Section: Gabaergic Systemmentioning

confidence: 99%