Development and spike timing–dependent plasticity of recurrent excitation in the Xenopus optic tectum

Much of the information processing in the brain occurs at the level of local circuits; however, the mechanisms underlying their initial development are poorly understood. We sought to examine the early development and plasticity of local excitatory circuits in the optic tectum of Xenopus laevis tadpoles. We found that retinal input recruits persistent, recurrent intratectal synaptic excitation that becomes more temporally compact and less variable over development, thus increasing the temporal coherence and precision of tectal cell spiking. We also saw that patterned retinal input can sculpt recurrent activity according to a spike timing–dependent plasticity rule, and that impairing this plasticity during development results in abnormal refinement of the temporal characteristics of recurrent circuits. This plasticity is a previously unknown mechanism by which patterned retinal activity allows intratectal circuitry to self-organize, optimizing the temporal response properties of the tectal network, and provides a substrate for rapid modulation of tectal neuron receptive-field properties.

[1]  W. C. Hall,et al.  Role of intrinsic synaptic circuitry in collicular sensorimotor integration. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[2]  D. McCormick,et al.  Postnatal development of synchronized network oscillations in the ferret dorsal lateral geniculate and perigeniculate nuclei , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  T. Isa,et al.  Local Excitatory Network and NMDA Receptor Activation Generate a Synchronous and Bursting Command from the Superior Colliculus , 2003, The Journal of Neuroscience.

[4]  M. Poo,et al.  Spike Timing-Dependent LTP/LTD Mediates Visual Experience-Dependent Plasticity in a Developing Retinotectal System , 2006, Neuron.

[5]  C. Akerman,et al.  Visually Driven Regulation of Intrinsic Neuronal Excitability Improves Stimulus Detection In Vivo , 2003, Neuron.

[6]  H. Cline,et al.  Visually Driven Modulation of Glutamatergic Synaptic Transmission Is Mediated by the Regulation of Intracellular Polyamines , 2002, Neuron.

[7]  Carlos D. Aizenman,et al.  Homeostatic Regulation of Intrinsic Excitability and Synaptic Transmission in a Developing Visual Circuit , 2007, The Journal of Neuroscience.

[8]  H. Nakagawa,et al.  Principal neuronal organization in the frog optic tectum revealed by a current source density analysis , 1997, Visual Neuroscience.

[9]  G. Laurent,et al.  Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts , 2007, Nature.

[10]  Y. Dan,et al.  Temporal Specificity in the Cortical Plasticity of Visual Space Representation , 2002, Science.

[11]  M A Xu-Friedman,et al.  Probing Fundamental Aspects of Synaptic Transmission with Strontium , 2000, The Journal of Neuroscience.

[12]  Mu-ming Poo,et al.  Activity-Dependent Matching of Excitatory and Inhibitory Inputs during Refinement of Visual Receptive Fields , 2005, Neuron.

[13]  E. S. Ruthazer,et al.  Control of Axon Branch Dynamics by Correlated Activity in Vivo , 2003, Science.

[14]  Hollis T. Cline,et al.  Glutamate Receptor Activity Is Required for Normal Development of Tectal Cell Dendrites In Vivo , 1998, The Journal of Neuroscience.

[15]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[16]  Pak-Ming Lau,et al.  Synaptic mechanisms of persistent reverberatory activity in neuronal networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Gurdon,et al.  Normal table of Xenopus laevis (Daudin) , 1995 .

[18]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[19]  Feng Qi Han,et al.  Rapid learning in cortical coding of visual scenes , 2007, Nature Neuroscience.

[20]  H. Cline,et al.  Enhanced visual activity in vivo forms nascent synapses in the developing retinotectal projection. , 2007, Journal of neurophysiology.

[21]  M. Carandini Amplification of Trial-to-Trial Response Variability by Neurons in Visual Cortex , 2004, PLoS biology.

[22]  D. Feldman,et al.  Modulation of spike timing by sensory deprivation during induction of cortical map plasticity , 2004, Nature Neuroscience.

[23]  C. Koch,et al.  Encoding of visual information by LGN bursts. , 1999, Journal of neurophysiology.

[24]  H. Cline,et al.  Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. , 1999, Journal of neurophysiology.

[25]  Nicholas J. Priebe,et al.  The contribution of spike threshold to the dichotomy of cortical simple and complex cells , 2004, Nature Neuroscience.

[26]  M. Sur,et al.  Development and plasticity of cortical areas and networks , 2001, Nature Reviews Neuroscience.

[27]  P. Usherwood,et al.  Inhibition of nicotinic acetylcholine receptor by philanthotoxin-343: kinetic investigations in the microsecond time region using a laser-pulse photolysis technique. , 1999, Biochemistry.

[28]  Florian Engert,et al.  Spatiotemporal Specificity of Neuronal Activity Directs the Modification of Receptive Fields in the Developing Retinotectal System , 2006, Neuron.

[29]  Dean V Buonomano,et al.  Timing of neural responses in cortical organotypic slices , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J E Lisman,et al.  Storage of 7 +/- 2 short-term memories in oscillatory subcycles , 1995, Science.

[31]  D. McCormick,et al.  Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition , 2006, The Journal of Neuroscience.

[32]  R. Malinow,et al.  In vivo development of neuronal structure and function. , 1996, Cold Spring Harbor symposia on quantitative biology.

[33]  E. Debski,et al.  Activity-dependent mapping in the retinotectal projection , 2002, Current Opinion in Neurobiology.

[34]  F Edward Dudek,et al.  Unmasking recurrent excitation generated by mossy fiber sprouting in the epileptic dentate gyrus: an emergent property of a complex system. , 2007, Progress in brain research.

[35]  O. Grüsser,et al.  Neurophysiology of the Anuran Visual System , 1976 .

[36]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  J. Faber,et al.  Normal Table of Xenopus Laevis (Daudin) , 1958 .

[38]  J D Clements,et al.  Detection of spontaneous synaptic events with an optimally scaled template. , 1997, Biophysical journal.

[39]  A. Peters,et al.  Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. , 1993, Cerebral cortex.

[40]  G. Lázár The development of the optic tectum in Xenopus laevis: a Golgi study. , 1973, Journal of anatomy.

[41]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

[42]  V. Jayaraman,et al.  How fast does the gamma-aminobutyric acid receptor channel open? Kinetic investigations in the microsecond time region using a laser-pulse photolysis technique. , 1999, Biochemistry.

[43]  R. Malinow,et al.  Maturation of a Central Glutamatergic Synapse , 1996, Science.

[44]  Peter Somogyi,et al.  Anti-Hebbian Long-Term Potentiation in the Hippocampal Feedback Inhibitory Circuit , 2007, Science.

[45]  John M. Beggs,et al.  Behavioral / Systems / Cognitive Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures , 2004 .

[46]  C. Akerman,et al.  Depolarizing GABAergic Conductances Regulate the Balance of Excitation to Inhibition in the Developing Retinotectal Circuit In Vivo , 2006, The Journal of Neuroscience.

[47]  G. Székely,et al.  Golgi studies on the optic center of the frog. , 1967, Journal fur Hirnforschung.

[48]  W. Smeets,et al.  Choline acetyltransferase immunoreactivity in the developing brain of Xenopus laevis , 2002, The Journal of comparative neurology.

[49]  S. Udin,et al.  The development of the nucleus isthmi in Xenopus laevis. I. Cell genesis and the formation of connections with the tectum , 1985, The Journal of comparative neurology.

[50]  G. P. Hess,et al.  On the mechanism of inhibition of the nicotinic acetylcholine receptor by the anticonvulsant MK-801 investigated by laser-pulse photolysis in the microsecond-to-millisecond time region. , 1999, Biochemistry.

[51]  William A. Harris,et al.  Order in the initial retinotectal map in Xenopus: a new technique for labelling growing nerve fibres , 1983, Nature.