Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period

By B. Chattopadhyaya, G. di Cristo, H. Higashiyama, G. Knott, S. Kuhlman, E. Welker, Z. J. Huang. Journal of Neuroscience, 2004

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The neocortical GABAergic network consists of diverse interneuron cell types that display distinct physiological properties and target their innervations to subcellular compartments of principal neurons. Inhibition directed toward the soma and proximal dendrites is crucial in regulating the output of pyramidal neurons, but the development of perisomatic innervation is poorly understood because of the lack of specific synaptic markers. In the primary visual cortex, for example, it is unknown whether, and to what extent, the formation and maturation of perisomatic synapses are intrinsic to cortical circuits or are regulated by sensory experience. Using bacterial artificial chromosome transgenic mice that label a defined class of perisomatic synapses with green fluorescent protein, here we show that perisomatic innervation developed during a protracted postnatal period after eye opening. Maturation of perisomatic innervation was significantly retarded by visual deprivation during the third, but not the fifth, postnatal week, implicating an important role for sensory input. To examine the role of cortical intrinsic mechanisms, we developed a method to visualize perisomatic synapses from single basket interneurons in cortical organotypic cultures. Characteristic perisomatic synapses formed through a stereotyped process, involving the extension of distinct terminal branches and proliferation of perisomatic boutons. Neuronal spiking in organotypic cultures was necessary for the proliferation of boutons and the extension, but not the maintenance, of terminal branches. Together, our results suggest that although the formation of perisomatic synapses is intrinsic to the cortex, visual experience can influence the maturation and pattern of perisomatic innervation during a postnatal critical period by modulating the level of neural activity within cortical circuits.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neurology

View Paper: https://www.semanticscholar.org/paper/082fcec66798cef471ca86cbb0076da98f1a9199

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Citations in the corpus

Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? (2011, methodology): “…or frontal coronal slices 350 m thick were prepared from P12– P17 (14.4 0.2), P22–P25 (22.8 0.5), and P31–P45 (35.5 3.3) G42 mice of either sex (Chattopadhyaya et al., 2004) using a Leica VT1000S or VT1200S vibratome with ice-cold sucrose solution containing the following (in mM): 27…”
Regulation of NMDA Receptor Subunit Expression and Its Implications for LTD, LTP, and Metaplasticity (2008, background): “…and inhibitory inputs are important contributors to the induction of plasticity (Choi et al., 2002; Steele and Mauk, 1999), and these factors are well known to vary with region and developmental stage (Chattopadhyaya et al., 2004; Jiang et al., 2005; Morales et al., 2002; Yasuda et al., 2003).”
The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors (2010, methodology): “For comparison, we also recorded FS from neurons as identified by EGFP expression in the B13 mouse.”
Dynamic Remodeling of Dendritic Arbors in GABAergic Interneurons of Adult Visual Cortex (2005, methodology): “030 ml/g IP) and their brains processed for immunohistochemistry essentially as described [51].”
Genetic dissection of neural circuits. (2008, positive): “Rather than expressing GFP in all GAD-positive inhibitory neurons, expression is restricted to diverse subsets of inhibitory neurons that are reproducible across animals within a single transgenic line (Oliva et al., 2000; Chattopadhyaya et al., 2004; Lopez-Bendito et al., 2004).”
One Rule to Grow Them All: A General Theory of Neuronal Branching and Its Practical Application (2010, background): “(B) Maximum intensity projections of tiled 2-photon fluorescent image stacks acquired at 820 nm from primary visual cortex of a p13 JAX transgenic mouse (strain # 007677, [38]) expressing GFP in parvalbumin interneurons,of which one is present.”
A Mammalian enhancer trap resource for discovering and manipulating neuronal cell types (2016, background): “Specifically, we tested four ultra conserved, non-coding sequences found to have forebrain enhancer activity in an embryonic screen (Visel et al., 2007) and four promoters—CamKII (Tsien et al., 1996), Gad1 (Chattopadhyaya et al., 2004; Szabo et al., 1996), Thy1 (Feng et al., 2000), and Slc32a (Ebiha”
Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons (2013, positive): “Transgenic mice used were: GAD67-GFP (all subpopulations of interneurons)[51], GIN (Sst cells)[52], G42 (Pvalb cells)[53], B13 (Pvalb cells)[39], HTR3a-GFP (Gensat#DH30) (VIP cells and others including layer 1) [25,43], ROSA-tdTomato[54], Pvalb-Cre[20], Sst-Cre[21], and VIP-Cre[21].”
Adolescence as a neurobiological critical period for the development of higher-order cognition (2018, neutral): “visual (Chattopadhyaya et al., 2004) and somatosensory systems (Micheva and Beaulieu, 1997)) is completed prior to adolescence (Huang et al.”
Aperiodic EEG and 7T MRSI evidence for maturation of E/I balance supporting the development of working memory through adolescence (2024, background): “Supporting this hypothesis are studies in rodent models (Chattopadhyaya et al., 2004; Micheva and Beaulieu, 1997) and postmortem human tissue (Mauney et al., 2013; Fung et al., 2010) that have shown mechanistic changes consistent with critical period plasticity, including increases in inhibitory,…”