XB-ART-54208
Neuron
2016 Jun 15;906:1203-1214. doi: 10.1016/j.neuron.2016.04.044.
Show Gene links
Show Anatomy links
Experience-Dependent Bimodal Plasticity of Inhibitory Neurons in Early Development.
???displayArticle.abstract???
Inhibitory neurons are heterogeneous in the mature brain. It is unclear when and how inhibitory neurons express distinct structural and functional profiles. Using in vivo time-lapse imaging of tectal neuron structure and visually evoked Ca(2+) responses in tadpoles, we found that inhibitory neurons cluster into two groups with opposite valence of plasticity after 4 hr of dark and visual stimulation. Half decreased dendritic arbor size and Ca(2+) responses after dark and increased them after visual stimulation, matching plasticity in excitatory neurons. Half increased dendrite arbor size and Ca(2+) responses following dark and decreased them after stimulation. At the circuit level, visually evoked excitatory and inhibitory synaptic inputs were potentiated by visual experience and E/I remained constant. Our results indicate that developing inhibitory neurons fall into distinct functional groups with opposite experience-dependent plasticity and as such, are well positioned to foster experience-dependent synaptic plasticity and maintain circuit stability during labile periods of circuit development.
???displayArticle.pubmedLink??? 27238867
???displayArticle.pmcLink??? PMC4938159
???displayArticle.link??? Neuron
???displayArticle.grants??? [+]
R01 EY011261 NEI NIH HHS
References [+] :
Akerman,
Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo.
2006, Pubmed,
Xenbase
Akerman, Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. 2006, Pubmed , Xenbase
Anastasiades, GABAergic interneurons form transient layer-specific circuits in early postnatal neocortex. 2016, Pubmed
Antal, Distribution of GABA immunoreactivity in the optic tectum of the frog: a light and electron microscopic study. 1991, Pubmed
Antonini, Anatomical correlates of functional plasticity in mouse visual cortex. 1999, Pubmed
Ascoli, Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. 2008, Pubmed
Bartley, Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits. 2008, Pubmed
Basu, A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. 2013, Pubmed
Batista-Brito, The developmental integration of cortical interneurons into a functional network. 2009, Pubmed
Batista-Brito, Gene expression in cortical interneuron precursors is prescient of their mature function. 2008, Pubmed
Caputi, The long and short of GABAergic neurons. 2013, Pubmed
Carvalho, Differential effects of excitatory and inhibitory plasticity on synaptically driven neuronal input-output functions. 2009, Pubmed
Chattopadhyaya, Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. 2004, Pubmed
Chen, Neuronal structural remodeling: is it all about access? 2010, Pubmed
Chen, Structural basis for the role of inhibition in facilitating adult brain plasticity. 2011, Pubmed
Chen, Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning. 2015, Pubmed
Chen, Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. 2012, Pubmed
Chen, Ultrasensitive fluorescent proteins for imaging neuronal activity. 2013, Pubmed
Chklovskii, Cortical rewiring and information storage. 2004, Pubmed
Ciarleglio, Multivariate analysis of electrophysiological diversity of Xenopus visual neurons during development and plasticity. 2015, Pubmed , Xenbase
Cline, Dendritic arbor development and synaptogenesis. 2001, Pubmed
Cline, The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. 2008, Pubmed
Dobie, Inhibitory synapse dynamics: coordinated presynaptic and postsynaptic mobility and the major contribution of recycled vesicles to new synapse formation. 2011, Pubmed
Gabernet, Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. 2005, Pubmed
Gábriel, Calretinin-immunoreactive elements in the retina and optic tectum of the frog, Rana esculenta. 1998, Pubmed
Gibson, Two networks of electrically coupled inhibitory neurons in neocortex. 1999, Pubmed
Haider, Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. 2006, Pubmed
He, Diadem X: automated 4 dimensional analysis of morphological data. 2011, Pubmed
Hendry, Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. 1988, Pubmed
Hensch, Local GABA circuit control of experience-dependent plasticity in developing visual cortex. 1998, Pubmed
Holtmaat, Experience-dependent structural synaptic plasticity in the mammalian brain. 2009, Pubmed
Huang, BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. 1999, Pubmed
Huang, Development of GABA innervation in the cerebral and cerebellar cortices. 2007, Pubmed
Jiao, Major effects of sensory experiences on the neocortical inhibitory circuits. 2006, Pubmed
Katz, Synaptic activity and the construction of cortical circuits. 1996, Pubmed
Keck, Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. 2011, Pubmed
Kepecs, Interneuron cell types are fit to function. 2014, Pubmed
Khakhalin, Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles. 2014, Pubmed , Xenbase
Kirkwood, Elementary forms of synaptic plasticity in the visual cortex. 1995, Pubmed
Kreczko, Visual deprivation decreases somatic GAD65 puncta number on layer 2/3 pyramidal neurons in mouse visual cortex. 2009, Pubmed
Kuhlman, Fast-spiking interneurons have an initial orientation bias that is lost with vision. 2011, Pubmed
Kvitsiani, Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. 2013, Pubmed
Laquerriere, Distribution of somatostatin receptors in the brain of the frog Rana ridibunda: correlation with the localization of somatostatin-containing neurons. 1989, Pubmed
Lee, Computer aided alignment and quantitative 4D structural plasticity analysis of neurons. 2013, Pubmed , Xenbase
Letzkus, A disinhibitory microcircuit for associative fear learning in the auditory cortex. 2011, Pubmed
Levelt, Critical-period plasticity in the visual cortex. 2012, Pubmed
Li, In vivo time-lapse imaging and serial section electron microscopy reveal developmental synaptic rearrangements. 2011, Pubmed , Xenbase
Liu, Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. 2004, Pubmed
Lovett-Barron, Regulation of neuronal input transformations by tunable dendritic inhibition. 2012, Pubmed
Lu, Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. 2007, Pubmed
Maffei, Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. 2004, Pubmed
Maffei, Potentiation of cortical inhibition by visual deprivation. 2006, Pubmed
Marik, Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. 2010, Pubmed
McKay, Physiological and morphological development of the rat cerebellar Purkinje cell. 2005, Pubmed
Micheva, An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. 1995, Pubmed
Miraucourt, GABA expression and regulation by sensory experience in the developing visual system. 2012, Pubmed , Xenbase
Morales, Dark rearing alters the development of GABAergic transmission in visual cortex. 2002, Pubmed
Muldal, Clonal relationships impact neuronal tuning within a phylogenetically ancient vertebrate brain structure. 2014, Pubmed , Xenbase
Niell, Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. 2005, Pubmed
Pfeffer, Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. 2013, Pubmed
Podgorski, Functional clustering drives encoding improvement in a developing brain network during awake visual learning. 2012, Pubmed , Xenbase
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, Development and spike timing-dependent plasticity of recurrent excitation in the Xenopus optic tectum. 2008, Pubmed , Xenbase
Pratt, Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. 2007, Pubmed , Xenbase
Richards, GABAergic circuits control stimulus-instructed receptive field development in the optic tectum. 2010, Pubmed , Xenbase
Royer, Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. 2012, Pubmed
Ruthazer, Learning to see: patterned visual activity and the development of visual function. 2010, Pubmed
Rybicka, Ultrastructure and GABA immunoreactivity in layers 8 and 9 of the optic tectum of Xenopus laevis. 1994, Pubmed , Xenbase
Sanna, Distribution of parvalbumin immunoreactivity in the vertebrate retina. 1993, Pubmed
Sarro, Hearing loss alters the subcellular distribution of presynaptic GAD and postsynaptic GABAA receptors in the auditory cortex. 2008, Pubmed
Schuemann, Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation. 2013, Pubmed
Shen, Inhibition to excitation ratio regulates visual system responses and behavior in vivo. 2011, Pubmed , Xenbase
Song, Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. 2000, Pubmed
Stuesse, Immunohistochemical distribution of enkephalin, substance P, and somatostatin in the brainstem of the leopard frog, Rana pipiens. 2001, Pubmed
Takesian, Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity. 2010, Pubmed
Takesian, Hearing loss differentially affects thalamic drive to two cortical interneuron subtypes. 2013, Pubmed
Tao, Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. 2005, Pubmed , Xenbase
Tropea, Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. 2010, Pubmed
van Versendaal, Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. 2012, Pubmed
Wilson, Division and subtraction by distinct cortical inhibitory networks in vivo. 2012, Pubmed
Wolff, Amygdala interneuron subtypes control fear learning through disinhibition. 2014, Pubmed
Wu, Stabilization of dendritic arbor structure in vivo by CaMKII. 1998, Pubmed , Xenbase
Xu, Visual experience-dependent maturation of correlated neuronal activity patterns in a developing visual system. 2011, Pubmed , Xenbase
Xue, Equalizing excitation-inhibition ratios across visual cortical neurons. 2014, Pubmed
Zhou, Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. 2014, Pubmed