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J Neurophysiol
2011 Nov 01;1065:2285-302. doi: 10.1152/jn.00641.2011.
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Inhibition to excitation ratio regulates visual system responses and behavior in vivo.
Shen W
,
McKeown CR
,
Demas JA
,
Cline HT
.
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The balance of inhibitory to excitatory (I/E) synaptic inputs is thought to control information processing and behavioral output of the central nervous system. We sought to test the effects of the decreased or increased I/E ratio on visual circuit function and visually guided behavior in Xenopus tadpoles. We selectively decreased inhibitory synaptic transmission in optic tectal neurons by knocking down the γ2 subunit of the GABA(A) receptors (GABA(A)R) using antisense morpholino oligonucleotides or by expressing a peptide corresponding to an intracellular loop of the γ2 subunit, called ICL, which interferes with anchoring GABA(A)R at synapses. Recordings of miniature inhibitory postsynaptic currents (mIPSCs) and miniature excitatory PSCs (mEPSCs) showed that these treatments decreased the frequency of mIPSCs compared with control tectal neurons without affecting mEPSC frequency, resulting in an ∼50% decrease in the ratio of I/E synaptic input. ICL expression and γ2-subunit knockdown also decreased the ratio of optic nerve-evoked synaptic I/E responses. We recorded visually evoked responses from optic tectal neurons, in which the synaptic I/E ratio was decreased. Decreasing the synaptic I/E ratio in tectal neurons increased the variance of first spike latency in response to full-field visual stimulation, increased recurrent activity in the tectal circuit, enlarged spatial receptive fields, and lengthened the temporal integration window. We used the benzodiazepine, diazepam (DZ), to increase inhibitory synaptic activity. DZ increased optic nerve-evoked inhibitory transmission but did not affect evoked excitatory currents, resulting in an increase in the I/E ratio of ∼30%. Increasing the I/E ratio with DZ decreased the variance of first spike latency, decreased spatial receptive field size, and lengthened temporal receptive fields. Sequential recordings of spikes and excitatory and inhibitory synaptic inputs to the same visual stimuli demonstrated that decreasing or increasing the I/E ratio disrupted input/output relations. We assessed the effect of an altered I/E ratio on a visually guided behavior that requires the optic tectum. Increasing and decreasing I/E in tectal neurons blocked the tectally mediated visual avoidance behavior. Because ICL expression, γ2-subunit knockdown, and DZ did not directly affect excitatory synaptic transmission, we interpret the results of our study as evidence that partially decreasing or increasing the ratio of I/E disrupts several measures of visual system information processing and visually guided behavior in an intact vertebrate.
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
Alldred,
Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin.
2005,
Pubmed
Annaz,
Development of motion processing in children with autism.
2010,
Pubmed
Ascoli,
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex.
2008,
Pubmed
Berg,
Balanced inhibition and excitation drive spike activity in spinal half-centers.
2007,
Pubmed
Bestman,
In vivo single-cell electroporation for transfer of DNA and macromolecules.
2006,
Pubmed
,
Xenbase
Burkhalter,
Many specialists for suppressing cortical excitation.
2008,
Pubmed
Butts,
Temporal precision in the neural code and the timescales of natural vision.
2007,
Pubmed
Carvalho,
Differential effects of excitatory and inhibitory plasticity on synaptically driven neuronal input-output functions.
2009,
Pubmed
Davis,
Homeostatic control of neural activity: from phenomenology to molecular design.
2006,
Pubmed
Daw,
Rapid, activity-dependent plasticity in timing precision in neonatal barrel cortex.
2006,
Pubmed
Dong,
Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum.
2009,
Pubmed
,
Xenbase
Douglass,
Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons.
2008,
Pubmed
Engert,
Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons.
2002,
Pubmed
,
Xenbase
Essrich,
Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin.
1998,
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
Fritschy,
Pre- and post-synaptic mechanisms regulating the clustering of type A gamma-aminobutyric acid receptors (GABAA receptors).
2003,
Pubmed
Gabernet,
Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition.
2005,
Pubmed
Gahtan,
Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum.
2005,
Pubmed
Gandhi,
Delayed plasticity of inhibitory neurons in developing visual cortex.
2008,
Pubmed
Haas,
Targeted electroporation in Xenopus tadpoles in vivo--from single cells to the entire brain.
2002,
Pubmed
,
Xenbase
Haider,
Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition.
2006,
Pubmed
Haider,
Synaptic and network mechanisms of sparse and reliable visual cortical activity during nonclassical receptive field stimulation.
2010,
Pubmed
Hasenstaub,
Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks.
2005,
Pubmed
Heil,
First-spike latency of auditory neurons revisited.
2004,
Pubmed
Hensch,
Critical period plasticity in local cortical circuits.
2005,
Pubmed
Hicks,
Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition.
1983,
Pubmed
Houweling,
Behavioural report of single neuron stimulation in somatosensory cortex.
2008,
Pubmed
Jacob,
GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition.
2008,
Pubmed
Johansson,
First spikes in ensembles of human tactile afferents code complex spatial fingertip events.
2004,
Pubmed
Kremkow,
Functional consequences of correlated excitatory and inhibitory conductances in cortical networks.
2010,
Pubmed
Lee,
Neurodevelopmental effects of chronic exposure to elevated levels of pro-inflammatory cytokines in a developing visual system.
2010,
Pubmed
,
Xenbase
Lesica,
Adaptation to stimulus contrast and correlations during natural visual stimulation.
2007,
Pubmed
Li,
Burst spiking of a single cortical neuron modifies global brain state.
2009,
Pubmed
Liu,
Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites.
2004,
Pubmed
Liu,
Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage.
2007,
Pubmed
,
Xenbase
Liu,
Intervening inhibition underlies simple-cell receptive field structure in visual cortex.
2010,
Pubmed
Maffei,
Potentiation of cortical inhibition by visual deprivation.
2006,
Pubmed
Mainen,
Reliability of spike timing in neocortical neurons.
1995,
Pubmed
Marco,
Sensory processing in autism: a review of neurophysiologic findings.
2011,
Pubmed
Marder,
Timing and balance of inhibition enhance the effect of long-term potentiation on cell firing.
2004,
Pubmed
Meier,
Preferential accumulation of GABAA receptor gamma 2L, not gamma 2S, cytoplasmic loops at rat spinal cord inhibitory synapses.
2004,
Pubmed
Mittmann,
Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells.
2005,
Pubmed
Mody,
Diversity of inhibitory neurotransmission through GABA(A) receptors.
2004,
Pubmed
Moore,
Dynamics of neuronal processing in rat somatosensory cortex.
1999,
Pubmed
Morales,
Dark rearing alters the development of GABAergic transmission in visual cortex.
2002,
Pubmed
Mu,
Spike timing-dependent LTP/LTD mediates visual experience-dependent plasticity in a developing retinotectal system.
2006,
Pubmed
,
Xenbase
Nowak,
Spatial and temporal features of synaptic to discharge receptive field transformation in cat area 17.
2010,
Pubmed
Orger,
Control of visually guided behavior by distinct populations of spinal projection neurons.
2008,
Pubmed
Pagliardini,
Active expiration induced by excitation of ventral medulla in adult anesthetized rats.
2011,
Pubmed
Petersen,
Population coding in somatosensory cortex.
2002,
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
Priebe,
Inhibition, spike threshold, and stimulus selectivity in primary visual cortex.
2008,
Pubmed
Pronych,
Optomotor behaviour in Xenopus laevis tadpoles as a measure of the effect of gravity on visual and vestibular neural integration.
1996,
Pubmed
,
Xenbase
Prusky,
Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex.
2004,
Pubmed
Richards,
GABAergic circuits control stimulus-instructed receptive field development in the optic tectum.
2010,
Pubmed
,
Xenbase
Rubenstein,
Model of autism: increased ratio of excitation/inhibition in key neural systems.
2003,
Pubmed
Rumpel,
Postsynaptic receptor trafficking underlying a form of associative learning.
2005,
Pubmed
Ruthazer,
Learning to see: patterned visual activity and the development of visual function.
2010,
Pubmed
Sanna,
Changes in expression and function of extrasynaptic GABAA receptors in the rat hippocampus during pregnancy and after delivery.
2009,
Pubmed
Schweizer,
The gamma 2 subunit of GABA(A) receptors is required for maintenance of receptors at mature synapses.
2003,
Pubmed
Shen,
Type A GABA-receptor-dependent synaptic transmission sculpts dendritic arbor structure in Xenopus tadpoles in vivo.
2009,
Pubmed
,
Xenbase
Sieghart,
Subunit composition, distribution and function of GABA(A) receptor subtypes.
2002,
Pubmed
Sigel,
Mapping of the benzodiazepine recognition site on GABA(A) receptors.
2002,
Pubmed
Sillito,
The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat.
1975,
Pubmed
Stokes,
From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex.
2010,
Pubmed
Tang,
Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism.
2011,
Pubmed
Tao,
Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields.
2005,
Pubmed
,
Xenbase
Tiesinga,
Regulation of spike timing in visual cortical circuits.
2008,
Pubmed
Tucker,
Luminance-evoked inhibition in primary visual cortex: a transient veto of simultaneous and ongoing response.
2006,
Pubmed
Tye,
Amygdala circuitry mediating reversible and bidirectional control of anxiety.
2011,
Pubmed
Vislay-Meltzer,
Spatiotemporal specificity of neuronal activity directs the modification of receptive fields in the developing retinotectal system.
2006,
Pubmed
,
Xenbase
Wang,
GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation.
2003,
Pubmed
Wehr,
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex.
2003,
Pubmed
Witten,
Cholinergic interneurons control local circuit activity and cocaine conditioning.
2010,
Pubmed
Zhang,
Visual input induces long-term potentiation of developing retinotectal synapses.
2000,
Pubmed
,
Xenbase
Zhang,
Topography and synaptic shaping of direction selectivity in primary auditory cortex.
2003,
Pubmed
Zhang,
The MeCP2-null mouse hippocampus displays altered basal inhibitory rhythms and is prone to hyperexcitability.
2008,
Pubmed
