Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
???displayArticle.abstract???
The circuit controlling visually guided behavior in nonmammalian vertebrates, such as Xenopus tadpoles, includes retinal projections to the contralateral optic tectum, where visual information is processed, and tectal motor outputs projecting ipsilaterally to hindbrain and spinal cord. Tadpoles have an intertectal commissure whose function is unknown, but it might transfer information between the tectal lobes. Differences in visual experience between the two eyes have profound effects on the development and function of visual circuits in animals with binocular vision, but the effects on animals with fully crossed retinal projections are not clear. We tested the effect of monocular visual experience on the visuomotor circuit in Xenopus tadpoles. We show that cutting the intertectal commissure or providing visual experience to one eye (monocular visual experience) is sufficient to disrupt tectally mediated visual avoidance behavior. Monocular visual experience induces asymmetry in tectal circuit activity across the midline. Repeated exposure to monocular visual experience drives maturation of the stimulated retinotectal synapses, seen as increased AMPA-to-NMDA ratios, induces synaptic plasticity in intertectal synaptic connections, and induces bilaterally asymmetric changes in the tectal excitation-to-inhibition ratio (E/I). We show that unilateral expression of peptides that interfere with AMPA or GABAA receptor trafficking alters E/I in the transfected tectum and is sufficient to degrade visuomotor behavior. Our study demonstrates that monocular visual experience in animals with fully crossed visual systems produces asymmetric circuit function across the midline and degrades visuomotor behavior. The data further suggest that intertectal inputs are an integral component of a bilateral visuomotor circuit critical for behavior. NEW & NOTEWORTHY The developing optic tectum of Xenopus tadpoles represents a unique circuit in which laterally positioned eyes provide sensory input to a circuit that is transiently monocular, but which will be binocular in the animal's adulthood. We challenge the idea that the two lobes of tadpole optic tectum function independently by testing the requirement of interhemispheric communication and demonstrate that unbalanced sensory input can induce structural and functional plasticity in the tectum sufficient to disrupt function.
Aizenman,
Enhanced visual activity in vivo forms nascent synapses in the developing retinotectal projection.
2007, Pubmed,
Xenbase
Aizenman,
Enhanced visual activity in vivo forms nascent synapses in the developing retinotectal projection.
2007,
Pubmed
,
Xenbase
Aizenman,
Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines.
2002,
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
Cooke,
How the mechanisms of long-term synaptic potentiation and depression serve experience-dependent plasticity in primary visual cortex.
2014,
Pubmed
COWAN,
An experimental study of the avian visual system.
1961,
Pubmed
D'amour,
Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex.
2015,
Pubmed
Deeg,
Development of multisensory convergence in the Xenopus optic tectum.
2009,
Pubmed
,
Xenbase
Dong,
Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum.
2009,
Pubmed
,
Xenbase
Dunn,
Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish.
2016,
Pubmed
Edwards,
The commissural projection of the superior colliculus in the cat.
1977,
Pubmed
Engert,
Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons.
2002,
Pubmed
,
Xenbase
Espinosa,
Development and plasticity of the primary visual cortex.
2012,
Pubmed
Fagiolini,
Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling.
2003,
Pubmed
Felch,
Multisensory integration in the developing tectum is constrained by the balance of excitation and inhibition.
2016,
Pubmed
,
Xenbase
Feldman,
The spike-timing dependence of plasticity.
2012,
Pubmed
Foa,
The scaffold protein, Homer1b/c, regulates axon pathfinding in the central nervous system in vivo.
2001,
Pubmed
,
Xenbase
Fong,
Rapid recovery from the effects of early monocular deprivation is enabled by temporary inactivation of the retinas.
2016,
Pubmed
Freeman,
Brief periods of monocular deprivation in kittens: effects of delay prior to physiological study.
1982,
Pubmed
Fritschy,
Epilepsy, E/I Balance and GABA(A) Receptor Plasticity.
2008,
Pubmed
Froemke,
Plasticity of cortical excitatory-inhibitory balance.
2015,
Pubmed
Gambrill,
Experience-dependent plasticity of excitatory and inhibitory intertectal inputs in Xenopus tadpoles.
2016,
Pubmed
,
Xenbase
Grant,
Changing patterns of binocular visual connections in the intertectal system during development of the frog, Xenopus laevis. I. Normal maturational changes in response to changing binocular geometry.
1989,
Pubmed
,
Xenbase
Gray,
A pair of motion-sensitive neurons in the locust encode approaches of a looming object.
2010,
Pubmed
Haas,
AMPA receptors regulate experience-dependent dendritic arbor growth in vivo.
2006,
Pubmed
,
Xenbase
Haas,
Targeted electroporation in Xenopus tadpoles in vivo--from single cells to the entire brain.
2002,
Pubmed
,
Xenbase
He,
Experience-Dependent Bimodal Plasticity of Inhibitory Neurons in Early Development.
2016,
Pubmed
,
Xenbase
He,
Experience-dependent recovery of vision following chronic deprivation amblyopia.
2007,
Pubmed
He,
Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex.
2006,
Pubmed
Hensch,
Excitatory-inhibitory balance and critical period plasticity in developing visual cortex.
2005,
Pubmed
Hensch,
Local GABA circuit control of experience-dependent plasticity in developing visual cortex.
1998,
Pubmed
Herrero,
Tectotectal connectivity in goldfish.
1999,
Pubmed
Hiramoto,
Convergence of multisensory inputs in Xenopus tadpole tectum.
2009,
Pubmed
,
Xenbase
Hiramoto,
Optic flow instructs retinotopic map formation through a spatial to temporal to spatial transformation of visual information.
2014,
Pubmed
,
Xenbase
Hubel,
Plasticity of ocular dominance columns in monkey striate cortex.
1977,
Pubmed
Hübener,
Neuronal plasticity: beyond the critical period.
2014,
Pubmed
Iwai,
Rapid critical period induction by tonic inhibition in visual cortex.
2003,
Pubmed
Jiang,
Maturation of GABAergic transmission and the timing of plasticity in visual cortex.
2005,
Pubmed
Keating,
The ipsilateral retinotectal pathway in the frog.
1970,
Pubmed
Khakhalin,
Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles.
2014,
Pubmed
,
Xenbase
King,
The superior colliculus.
2004,
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,
Fragile X Mental Retardation Protein Is Required to Maintain Visual Conditioning-Induced Behavioral Plasticity by Limiting Local Protein Synthesis.
2016,
Pubmed
,
Xenbase
Liu,
Early development and function of the Xenopus tadpole retinotectal circuit.
2016,
Pubmed
,
Xenbase
Liu,
Neuronal responses to looming objects in the superior colliculus of the cat.
2011,
Pubmed
Ma,
Downregulation of cortical inhibition mediates ocular dominance plasticity during the critical period.
2013,
Pubmed
Maffei,
Potentiation of cortical inhibition by visual deprivation.
2006,
Pubmed
McKeown,
Neurogenesis is required for behavioral recovery after injury in the visual system of Xenopus laevis.
2013,
Pubmed
,
Xenbase
Miraucourt,
GABA expression and regulation by sensory experience in the developing visual system.
2012,
Pubmed
,
Xenbase
Mitchell,
The case from animal studies for balanced binocular treatment strategies for human amblyopia.
2014,
Pubmed
Mu,
Spike timing-dependent LTP/LTD mediates visual experience-dependent plasticity in a developing retinotectal system.
2006,
Pubmed
,
Xenbase
Munz,
Rapid Hebbian axonal remodeling mediated by visual stimulation.
2014,
Pubmed
,
Xenbase
Murphy,
Development of human visual cortex: a balance between excitatory and inhibitory plasticity mechanisms.
2005,
Pubmed
Pietrasanta,
The corpus callosum and the visual cortex: plasticity is a game for two.
2012,
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
Pratt,
Development and spike timing-dependent plasticity of recurrent excitation in the Xenopus optic tectum.
2008,
Pubmed
,
Xenbase
Pratt,
Multisensory integration in mesencephalic trigeminal neurons in Xenopus tadpoles.
2009,
Pubmed
,
Xenbase
Pratt,
An Evolutionarily Conserved Mechanism for Activity-Dependent Visual Circuit Development.
2016,
Pubmed
Richards,
In vivo spike-timing-dependent plasticity in the optic tectum of Xenopus laevis.
2010,
Pubmed
,
Xenbase
Richards,
GABAergic circuits control stimulus-instructed receptive field development in the optic tectum.
2010,
Pubmed
,
Xenbase
Ruthazer,
Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective.
2004,
Pubmed
Ruthazer,
Stabilization of axon branch dynamics by synaptic maturation.
2006,
Pubmed
,
Xenbase
Ruthazer,
Learning to see: patterned visual activity and the development of visual function.
2010,
Pubmed
Santer,
Predator versus prey: locust looming-detector neuron and behavioural responses to stimuli representing attacking bird predators.
2012,
Pubmed
Sharma,
The retinal projections in the goldfish: an experimental study.
1972,
Pubmed
Shen,
Acute synthesis of CPEB is required for plasticity of visual avoidance behavior in Xenopus.
2014,
Pubmed
,
Xenbase
Shen,
Inhibition to excitation ratio regulates visual system responses and behavior in vivo.
2011,
Pubmed
,
Xenbase
Shen,
Type A GABA-receptor-dependent synaptic transmission sculpts dendritic arbor structure in Xenopus tadpoles in vivo.
2009,
Pubmed
,
Xenbase
Shi,
Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons.
2001,
Pubmed
Sin,
Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases.
2002,
Pubmed
,
Xenbase
Sprague,
Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat.
1966,
Pubmed
Sprekeler,
Functional consequences of inhibitory plasticity: homeostasis, the excitation-inhibition balance and beyond.
2017,
Pubmed
Takahashi,
Commissural mirror-symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements.
2007,
Pubmed
Tao,
Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields.
2005,
Pubmed
,
Xenbase
Tatti,
Neurophysiology and Regulation of the Balance Between Excitation and Inhibition in Neocortical Circuits.
2017,
Pubmed
Temizer,
A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish.
2015,
Pubmed
Tiesinga,
Regulation of spike timing in visual cortical circuits.
2008,
Pubmed
Tsui,
A developmental sensitive period for spike timing-dependent plasticity in the retinotectal projection.
2010,
Pubmed
,
Xenbase
Udin,
Binocular maps in Xenopus tectum: Visual experience and the development of isthmotectal topography.
2012,
Pubmed
,
Xenbase
Vislay-Meltzer,
Spatiotemporal specificity of neuronal activity directs the modification of receptive fields in the developing retinotectal system.
2006,
Pubmed
,
Xenbase
Vogels,
Inhibitory synaptic plasticity: spike timing-dependence and putative network function.
2013,
Pubmed
Waleszczyk,
Influence of the intertectal connection upon visual responses in the cat's superior colliculus.
1993,
Pubmed
Wallace,
Rats maintain an overhead binocular field at the expense of constant fusion.
2013,
Pubmed
Wang,
Critical period plasticity matches binocular orientation preference in the visual cortex.
2010,
Pubmed
WIESEL,
SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE.
1963,
Pubmed
Wu,
Tectal neurons signal impending collision of looming objects in the pigeon.
2005,
Pubmed
Zhang,
A critical window for cooperation and competition among developing retinotectal synapses.
1998,
Pubmed
,
Xenbase
Zhao,
Visual cortex modulates the magnitude but not the selectivity of looming-evoked responses in the superior colliculus of awake mice.
2014,
Pubmed
