Miraucourt LS , Silva JS , Burgos K , Li J , Abe H , Ruthazer ES , Cline HT .

EY011261 NEI NIH HHS , MOP-77567 ASPE HHS, R01 EY011261 NEI NIH HHS , R01 EY011261-16 NEI NIH HHS

	Figure 1. Immunocharacterization of stage 47 Xenopus laevis visual system.A. GABA immunofluorescent labeling in 200 nm LR White-embedded horizontal sections of optic tectum. GABA-positive somata are scattered throughout the cell body layer (CBL) and constitute the majority of neurons in the tectal neuropil (TN). The proliferative cells lining the ventricle (V) and in caudal tectum are not GABA immunoreactive. B. Ultrastructure of GABAergic synapses identified by post-embedding immunogold labeling in 70 nm sections from epoxy-resin embedded tissue. Electron micrograph of the tectal neuropil, showing two GABAergic presynaptic profiles forming symmetric contacts with a non-GABAergic postsynaptic profile (solid arrows). On the right a postsynaptic profile receives an asymmetric, non-GABAergic synaptic input with a prominent postsynaptic density (hollow arrows). C. Size comparison for GABA-negative (N = 28) and GABA-positive (N = 12) post-synaptic profiles (PSPs) and presynaptic terminals. D–F. Cryosections through optic tectum immunostained for αCaMKII (D) and GABA (E), and the merge of a CaMKII (red) and GABA (green) immunolabeling (F). There is little overlap of the CaMKII- and GABA-immunolabeled cells. G–I. αCaMKII (G) and GABA (H) immunolabeling in the retina. Most RGCs are αCaMKII immunoreactive. Neurons in the INL are predominately GABA-immunoreactive. Double labeling the retina for αCaMKII (H) and GABA (I) immunopositive cells shows little overlap in the cell body layers. J–L. Immunostaining for glycine and GABA reveals no detectable glycine label in the tectum (J). M–O. In the retina glycine-positive amacrine cells (M) are prominent in the INL (red in O) and are distinct from the GABAergic amacrine cells (N), shown as green in O. A few GABA-positive displaced amacrine cell bodies are also found in the ganglion cell layer (H, I, N, O). P–R. Immunolabeling for glycine (P, red in R) and GABA (Q, green in R) in the spinal cord shows neurons in the spinal cord can be immunoreactive for both transmitters (R). Scale Bars in A: 150 µm, in B: 500 nm, in D, G, J, M, and P: 50 µm, and apply to all images in the corresponding row.
	Figure 2. Distribution of GABA immunoreactivity in stage 42 and stage 47 tadpole CNS.A. Stage 42: Schematic (left) indicating relative positions of montaged sagittal sections of the tadpole brain. Blue is the cell body area; white is the neuropil area. Sections (1–4) show GABA immunostaining (green) counterstained with the nuclear label, propidium iodide (PI, blue). GABA staining alone is presented in the right panels (1′–4′). In panels 1′–4′ arrowheads indicate GABA containing somata, filled arrows are GABA-positive axon tracts, and open arrows denote GABA-sparse zones. B. Sagittal series through a stage 47 tadpole brain. The pattern of GABA-immunoreactivity in the brain is similar to stage 42 except for a dispersion of the dense clusters of GABA immunoreactive cells seen in younger brains and the vast expansion of the labeled cell body regions, neuropil and axon tracts in the older tadpoles. Scale bars, 250 µm. See text for details.
	Figure 3. GABA immunoreactivity in optic tectum of stage 42 and stage 47 tadpoles (horizontal plane).A. Stage 42: Left: Schematic indicating relative positions of horizontal sections through the dorsal midbrain and locations of major brain regions (top left). Schematic of a horizontal section through the brain with locations of brain regions labeled. Blue is the cell body area; white is the neuropil area. An image of a GABA-immunolabeled right hemisection is superimposed on the schematic (bottom left). Sections (1–5) show GABA-immunoreactivity (green) counterstained with PI (blue). B. Schematic of horizontal brain section (left) showing regions of high magnification images, shown to the right. Higher magnification single optical sections from stage 42 midbrain. B1. Intense GABA immunolabeling of axons in the tecto-tegmental commissure (ttc) and posterior commissure (pc) (solid arrows). B2. Clustered GABA-immunoreactive neurons in the optic tectum (solid arrows) extend processes toward the neuropil. B2a, b. Enlargements of boxed regions in B2 showing GABA-immunoreactive processes (arrows) extending from labeled cell bodies (arrowheads in 2a,b). C. Stage 47: Left. Schematics comparable to A. Sections (1–5) of GABA-immunoreactivity (green) and PI counterstain (blue). GABA-immunoreactivity becomes more broadly distributed across the optic tectal cell body layer (arrowheads) and neuropil. D. Higher magnification (single optical sections) showing strong GABA labeling in the lateral forebrain bundle (lfb, D1), and sparse GABA-positive somata in the caudolateral optic tectum (D2a, arrowheads) extending GABA-positive processes toward the neuropil (D2a, solid arrows). D3. The border between the caudal optic tectum and the medial hindbrain (HB) shows that the proliferative zone in caudal tectum is negative for GABA immunostaining (arrows), whereas neuronal cell bodies and processes in the medial HB are GABA-immunolabeled (arrowheads). Scale bars, A, C: 50 µm; B1, 2: 20 µm; B2a,b: 10 µm: D1,3: 30 µm; D2a,b: 20 µm.
	Figure 4. GABA immunoreactivity in optic tectum of stage 42 and stage 47 tadpoles (coronal plane).A. Stage 42: Left: Schematic indicating relative positions of coronal sections through the midbrain. Right: Sections (1–4) show GABA immunoreactivity (green) with PI counterstain (blue). Schematics under each section identify major brain regions in the sections. Blue is the cell body area; white is the neuropil area. GABA-positive cells are clustered medially in the anterior tectum (arrowheads) and send processes to the neuropil (solid arrows; section 1). A cluster of GABA-labeled neurons extends from the anterior ventricular region posteriorly and laterally within the tectum (sections 1–3, arrowheads). GABA-positive neurons are dispersed in caudal tectum (section 4, arrowhead). The tegmentum of stage 42 tadpoles has relatively few GABA-immunoreactive neurons (open arrows, sections 1–4), but extensive GABA-immunoreactivity in the lateral neuropil. B. Stage 47: Schematics shown are comparable to those in A. GABA-positive cells are interspersed throughout the optic tectum dorsally and in the tegmentum. The labeled neurons are distributed more laterally than in the younger tadpoles (arrowheads; sections 1–4). The zone closest to the tectal ventricle is largely devoid of GABA-immunoreactivity (section 2, hollow arrow). The tectal and tegmental neuropil regions are intensely GABA immunoreactive. Scale bar, 50 µm.
	Figure 5. GABA immunoreactvity in retina of stage 42 and stage 47 tadpoles.A. Stage 42 coronal cryosection of the retina showing GABA immunoreactivity (green) and propidium iodide (blue) staining in the retina. B. GABA immunolabeling alone. At this stage, GABA immunolabeling is absent from the ganglion cell layer (GCL, hollow arrow) and outer nuclear label (ONL, hollow arrow). GABA-positive cell somata are densely packed in the INL and ramify processes into the GCL (solid arrow) and OPL (solid arrow). D. Stage 47 sections through retina showing GABA immunoreactivity (green) and propidium iodide counterstain (blue). A few GABA-positive somata are now evident in the GCL (arrowheads). GABA immunoreactivity is present in the IPL, INL and OPL, but absent in the ONL. Scale bar, 25 µm.
	Figure 6. Modulation of GABA levels in the optic tectum by visual stimulation.A. Examples of cryosections from stage 47 midbrains immunostained for GABA and ßIII-tubulin. Tadpoles were either visually stimulated (n = 5) or kept in the dark (n = 4) for 4 hr. Scale bar, 100 µm. B. Animals exposed to visual stimulation had consistently higher levels of GABA immunoreactivity, normalized to ßIII tubulin, in both the neuropil and cell body layer compared to animals kept in the dark (*p<0.05, Student's t-test). C. Elisa measurements of GABA concentrations in homogenates of optic tectum are significantly higher in animals exposed to 4 hr of visual stimulation compared to animals kept in the dark.

Abraham, Metaplasticity: the plasticity of synaptic plasticity. 1996, Pubmed

Abraham, Metaplasticity: the plasticity of synaptic plasticity. 1996, Pubmed
Aizenman, Enhanced visual activity in vivo forms nascent synapses in the developing retinotectal projection. 2007, Pubmed , Xenbase
Aizenman, Visually driven regulation of intrinsic neuronal excitability improves stimulus detection in vivo. 2003, Pubmed , Xenbase
Akerman, Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. 2006, Pubmed , Xenbase
Akerman, Refining the roles of GABAergic signaling during neural circuit formation. 2007, Pubmed
Akhtar, Activity-dependent regulation of glutamic acid decarboxylase in the rat barrel cortex: effects of neonatal versus adult sensory deprivation. 1991, Pubmed
Ascoli, Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. 2008, Pubmed
Bachy, GABAergic specification in the basal forebrain is controlled by the LIM-hd factor Lhx7. 2006, Pubmed , Xenbase
Bachy, Defining pallial and subpallial divisions in the developing Xenopus forebrain. 2002, Pubmed , Xenbase
Barale, Immunohistochemical investigation of gamma-aminobutyric acid ontogeny and transient expression in the central nervous system of Xenopus laevis tadpoles. 1996, Pubmed , Xenbase
Bartley, Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits. 2008, Pubmed
Ben-Ari, GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. 2007, Pubmed
Benevento, gamma-Aminobutyric acid and somatostatin immunoreactivity in the visual cortex of normal and dark-reared rats. 1995, Pubmed
Benson, Differential effects of monocular deprivation on glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase gene expression in the adult monkey visual cortex. 1991, Pubmed
Benson, Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+/calmodulin protein kinase gene expression in the rat central nervous system. 1992, Pubmed
Benson, Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal ganglia, thalamus, and hypothalamus of the monkey. 1991, Pubmed
Bertrand, Proneural genes and the specification of neural cell types. 2002, Pubmed
Bestman, In vivo time-lapse imaging of cell proliferation and differentiation in the optic tectum of Xenopus laevis tadpoles. 2012, Pubmed , Xenbase
Blankenship, Mechanisms underlying spontaneous patterned activity in developing neural circuits. 2010, Pubmed
Blitz, Timing and specificity of feed-forward inhibition within the LGN. 2005, Pubmed
Bonaventure, Neurotransmission in the frog retina: possible physiological and histological correlations. 1989, Pubmed
Borodinsky, Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. 2004, Pubmed , Xenbase
Brox, Expression of the genes GAD67 and Distal-less-4 in the forebrain of Xenopus laevis confirms a common pattern in tetrapods. 2003, Pubmed , Xenbase
Buddhala, A novel mechanism for GABA synthesis and packaging into synaptic vesicles. 2009, Pubmed
Chen, Amacrine-to-amacrine cell inhibition: Spatiotemporal properties of GABA and glycine pathways. 2011, Pubmed
Cohen-Cory, Brain-derived neurotrophic factor and the development of structural neuronal connectivity. 2010, Pubmed
Cohen-Cory, Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. 1995, Pubmed , Xenbase
Crair, Neuronal activity during development: permissive or instructive? 1999, Pubmed
Del Bene, Filtering of visual information in the tectum by an identified neural circuit. 2010, Pubmed
Desai, Critical periods for experience-dependent synaptic scaling in visual cortex. 2002, Pubmed
Dirkx, Targeting of the 67-kDa isoform of glutamic acid decarboxylase to intracellular organelles is mediated by its interaction with the NH2-terminal region of the 65-kDa isoform of glutamic acid decarboxylase. 1995, Pubmed
Dupuy, Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. 1996, Pubmed
Erondu, Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. 1985, Pubmed
Esclapez, Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. 1994, Pubmed
Fagiolini, Specific GABAA circuits for visual cortical plasticity. 2004, Pubmed
Farrant, Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. 2005, Pubmed
Fenalti, GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. 2007, Pubmed
Figdor, Segmental organization of embryonic diencephalon. 1993, Pubmed
Fiumelli, Role of activity-dependent regulation of neuronal chloride homeostasis in development. 2007, Pubmed
Fode, A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. 2000, Pubmed
Gabernet, Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. 2005, Pubmed
Goel, Phosphorylation of AMPA receptors is required for sensory deprivation-induced homeostatic synaptic plasticity. 2011, Pubmed
Goel, Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. 2007, Pubmed
Goel, Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. 2006, Pubmed
González, Regional expression of the homeobox gene NKX2-1 defines pallidal and interneuronal populations in the basal ganglia of amphibians. 2002, Pubmed , Xenbase
Hartman, Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. 2006, Pubmed
Hartmann, Fast homeostatic plasticity of inhibition via activity-dependent vesicular filling. 2008, Pubmed
He, Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. 2006, Pubmed
Hendry, Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. 1988, Pubmed
Hendry, Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. , Pubmed
Hensch, Local GABA circuit control of experience-dependent plasticity in developing visual cortex. 1998, Pubmed
Hollyfield, Retinal development: Time and order of appearance of specific neuronal properties. 1980, Pubmed , Xenbase
Hu, BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. 2005, Pubmed , Xenbase
Huang, Development of GABA innervation in the cerebral and cerebellar cortices. 2007, Pubmed
Huang, Dual expression of GABA or serotonin and dopamine in Xenopus amacrine cells is transient and may be regulated by laminar cues. 1998, Pubmed , Xenbase
Jin, Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. 2003, Pubmed
Jinno, Neuronal diversity in GABAergic long-range projections from the hippocampus. 2007, Pubmed
Kanaani, The hydrophilic isoform of glutamate decarboxylase, GAD67, is targeted to membranes and nerve terminals independent of dimerization with the hydrophobic membrane-anchored isoform, GAD65. 1999, Pubmed
Kilman, Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. 2002, Pubmed
Klausberger, Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. 2008, Pubmed
Kohara, A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. 2007, Pubmed
Kreczko, Visual deprivation decreases somatic GAD65 puncta number on layer 2/3 pyramidal neurons in mouse visual cortex. 2009, Pubmed
Lázár, The development of the optic tectum in Xenopus laevis: a Golgi study. 1973, Pubmed , Xenbase
Li, Visual deprivation increases accumulation of dense core vesicles in developing optic tectal synapses in Xenopus laevis. 2010, Pubmed , Xenbase
Li, Distribution of GABA-like immunoreactive neurons and fibers in the central visual nuclei and retina of frog, Rana pipiens. 1998, Pubmed
Lien, Visual stimuli-induced LTD of GABAergic synapses mediated by presynaptic NMDA receptors. 2006, Pubmed , Xenbase
Lin, Activity-dependent regulation of inhibitory synapse development by Npas4. 2008, Pubmed
Lisman, The molecular basis of CaMKII function in synaptic and behavioural memory. 2002, Pubmed
Maffei, The age of plasticity: developmental regulation of synaptic plasticity in neocortical microcircuits. 2008, Pubmed
Maffei, Potentiation of cortical inhibition by visual deprivation. 2006, Pubmed
Marc, A molecular phenotype atlas of the zebrafish retina. 2001, Pubmed
Marder, Modeling stability in neuron and network function: the role of activity in homeostasis. 2002, Pubmed
Marder, Memory from the dynamics of intrinsic membrane currents. 1996, Pubmed
Marín, A long, remarkable journey: tangential migration in the telencephalon. 2001, Pubmed
Micheva, Development and plasticity of the inhibitory neocortical circuitry with an emphasis on the rodent barrel field cortex: a review. 1997, Pubmed
Micheva, Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. 1996, Pubmed
Micheva, Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. 2007, Pubmed
Micheva, An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. 1995, Pubmed
Micheva, Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA-immunoreactive neurons in the rat barrel field cortex. 1995, Pubmed
Miyashita, GABAergic projections from the hippocampus to the retrosplenial cortex in the rat. 2007, Pubmed
Morales, Dark rearing alters the development of GABAergic transmission in visual cortex. 2002, Pubmed
Mosinger, GABA-like immunoreactivity in the vertebrate retina: a species comparison. 1986, Pubmed
Mrsic-Flogel, Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. 2007, Pubmed
Mueller, A phylotypic stage in vertebrate brain development: GABA cell patterns in zebrafish compared with mouse. 2006, Pubmed , Xenbase
Ohba, BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. 2005, Pubmed
Parras, Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. 2002, Pubmed
Peng, Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling. 2010, Pubmed
Pouille, Input normalization by global feedforward inhibition expands cortical dynamic range. 2009, Pubmed
Pouille, Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. 2001, Pubmed
Pratt, Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. 2007, Pubmed , Xenbase
Puelles, Forebrain gene expression domains and the evolving prosomeric model. 2003, Pubmed
Reed, The spatial relationship of gamma-aminobutyric acid (GABA) neurons and gonadotropin-releasing hormone (GnRH) neurons in larval and adult sea lamprey, Petromyzon marinus. 2002, Pubmed
Richards, GABAergic circuits control stimulus-instructed receptive field development in the optic tectum. 2010, Pubmed , Xenbase
Roberts, The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. 1987, Pubmed , Xenbase
Robertson, Afferents of the lamprey optic tectum with special reference to the GABA input: combined tracing and immunohistochemical study. 2006, Pubmed
Robertson, GABA distribution in lamprey is phylogenetically conserved. 2007, Pubmed
Robles, Characterization of genetically targeted neuron types in the zebrafish optic tectum. 2011, Pubmed
Root, Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. 2008, Pubmed , Xenbase
Ruthazer, Learning to see: patterned visual activity and the development of visual function. 2010, Pubmed
Ruthazer, Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. 2004, Pubmed
Rybicka, Ultrastructure and GABA immunoreactivity in layers 8 and 9 of the optic tectum of Xenopus laevis. 1994, Pubmed , Xenbase
Sanchez, BDNF increases synapse density in dendrites of developing tectal neurons in vivo. 2006, Pubmed , Xenbase
Sánchez-Huertas, CREB-Dependent Regulation of GAD65 Transcription by BDNF/TrkB in Cortical Interneurons. 2011, Pubmed
Schwartz, Activity-dependent transcription of BDNF enhances visual acuity during development. 2011, Pubmed , Xenbase
Sharma, Visual activity regulates neural progenitor cells in developing xenopus CNS through musashi1. 2010, Pubmed , Xenbase
Shen, Type A GABA-receptor-dependent synaptic transmission sculpts dendritic arbor structure in Xenopus tadpoles in vivo. 2009, Pubmed , Xenbase
Shen, Inhibition to excitation ratio regulates visual system responses and behavior in vivo. 2011, Pubmed , Xenbase
Sin, Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. 2002, Pubmed , Xenbase
Stellwagen, Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. 2005, Pubmed
Tao, Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. 2005, Pubmed , Xenbase
Tighilet, Cell-specific expression of type II calcium/calmodulin-dependent protein kinase isoforms and glutamate receptors in normal and visually deprived lateral geniculate nucleus of monkeys. 1998, Pubmed
Tomioka, Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. 2007, Pubmed
Turrigiano, Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. 2011, Pubmed
Wässle, Glycinergic transmission in the Mammalian retina. 2009, Pubmed
Werblin, Six different roles for crossover inhibition in the retina: correcting the nonlinearities of synaptic transmission. 2010, Pubmed
Wonders, The origin and specification of cortical interneurons. 2006, Pubmed
Wong, Activity-dependent regulation of dendritic growth and patterning. 2002, Pubmed
Wu, Maturation of a central glutamatergic synapse. 1996, Pubmed , Xenbase
Wullimann, Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression. 2005, Pubmed , Xenbase
Zhang, Visual input induces long-term potentiation of developing retinotectal synapses. 2000, Pubmed , Xenbase