Literature DB >> 11157082

The information content of spontaneous retinal waves.

D A Butts1, D S Rokhsar.   

Abstract

Spontaneous neural activity that is present in the mammalian retina before the onset of vision is required for the refinement of retinotopy in the lateral geniculate nucleus and superior colliculus. This paper explores the information content of this retinal activity, with the goal of determining constraints on the nature of the developmental mechanisms that use it. Through information-theoretic analysis of multielectrode and calcium-imaging experiments, we show that the spontaneous retinal activity present early in development provides information about the relative positions of retinal ganglion cells and can, in principle, be used at retinogeniculate and retinocollicular synapses to refine retinotopy. Remarkably, we find that most retinotopic information provided by retinal waves exists on relatively coarse time scales, suggesting that developmental mechanisms must be sensitive to timing differences from 100 msec up to 2 sec to make optimal use of it. In fact, a simple Hebbian-type learning rule with a correlation window on the order of seconds is able to extract the bulk of the available information. These findings are consistent with bursts of action potentials (rather than single spikes) being the unit of information used during development and suggest new experimental approaches for studying developmental plasticity of the retinogeniculate and retinocollicular synapses. More generally, these results demonstrate how the properties of neuronal systems can be inferred from the statistics of their input.

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Year:  2001        PMID: 11157082      PMCID: PMC6762322     

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  35 in total

Review 1.  Information theory and neural coding.

Authors:  A Borst; F E Theunissen
Journal:  Nat Neurosci       Date:  1999-11       Impact factor: 24.884

2.  The role of retinal waves and synaptic normalization in retinogeniculate development.

Authors:  S J Eglen
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  1999-02-28       Impact factor: 6.237

3.  Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves.

Authors:  M B Feller; D P Wellis; D Stellwagen; F S Werblin; C J Shatz
Journal:  Science       Date:  1996-05-24       Impact factor: 47.728

4.  Topographic guidance labels in a sensory projection to the forebrain.

Authors:  D A Feldheim; P Vanderhaeghen; M J Hansen; J Frisén; Q Lu; M Barbacid; J G Flanagan
Journal:  Neuron       Date:  1998-12       Impact factor: 17.173

5.  Competition in retinogeniculate patterning driven by spontaneous activity.

Authors:  A A Penn; P A Riquelme; M B Feller; C J Shatz
Journal:  Science       Date:  1998-03-27       Impact factor: 47.728

6.  Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin.

Authors:  D W Sretavan; C J Shatz; M P Stryker
Journal:  Nature       Date:  1988-12-01       Impact factor: 49.962

Review 7.  Developmental mechanisms that generate precise patterns of neuronal connectivity.

Authors:  C S Goodman; C J Shatz
Journal:  Cell       Date:  1993-01       Impact factor: 41.582

8.  Transient period of correlated bursting activity during development of the mammalian retina.

Authors:  R O Wong; M Meister; C J Shatz
Journal:  Neuron       Date:  1993-11       Impact factor: 17.173

9.  N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map.

Authors:  D K Simon; G T Prusky; D D O'Leary; M Constantine-Paton
Journal:  Proc Natl Acad Sci U S A       Date:  1992-11-15       Impact factor: 11.205

10.  Development of topographic order in the mammalian retinocollicular projection.

Authors:  D K Simon; D D O'Leary
Journal:  J Neurosci       Date:  1992-04       Impact factor: 6.167

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  35 in total

1.  Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina.

Authors:  J H Singer; R R Mirotznik; M B Feller
Journal:  J Neurosci       Date:  2001-11-01       Impact factor: 6.167

2.  "Slow activity transients" in infant rat visual cortex: a spreading synchronous oscillation patterned by retinal waves.

Authors:  Matthew T Colonnese; Rustem Khazipov
Journal:  J Neurosci       Date:  2010-03-24       Impact factor: 6.167

3.  Development of precise maps in visual cortex requires patterned spontaneous activity in the retina.

Authors:  Jianhua Cang; René C Rentería; Megumi Kaneko; Xiaorong Liu; David R Copenhagen; Michael P Stryker
Journal:  Neuron       Date:  2005-12-08       Impact factor: 17.173

4.  Developmental period for N-methyl-D-aspartate (NMDA) receptor-dependent synapse elimination correlated with visuotopic map refinement.

Authors:  Matthew T Colonnese; Martha Constantine-Paton
Journal:  J Comp Neurol       Date:  2006-02-10       Impact factor: 3.215

5.  Neuronal pentraxins mediate synaptic refinement in the developing visual system.

Authors:  Lisa Bjartmar; Andrew D Huberman; Erik M Ullian; René C Rentería; Xiaoqin Liu; Weifeng Xu; Jennifer Prezioso; Michael W Susman; David Stellwagen; Caleb C Stokes; Richard Cho; Paul Worley; Robert C Malenka; Sherry Ball; Neal S Peachey; David Copenhagen; Barbara Chapman; Masaru Nakamoto; Ben A Barres; Mark S Perin
Journal:  J Neurosci       Date:  2006-06-07       Impact factor: 6.167

6.  Slow and fast pulses in 1-D cultures of excitatory neurons.

Authors:  E Alvarez-Lacalle; E Moses
Journal:  J Comput Neurosci       Date:  2009-01-24       Impact factor: 1.621

Review 7.  Synergy, redundancy, and multivariate information measures: an experimentalist's perspective.

Authors:  Nicholas Timme; Wesley Alford; Benjamin Flecker; John M Beggs
Journal:  J Comput Neurosci       Date:  2013-07-03       Impact factor: 1.621

8.  Self-organization in the developing nervous system: theoretical models.

Authors:  Stephen J Eglen; Julijana Gjorgjieva
Journal:  HFSP J       Date:  2009-03-23

Review 9.  Spontaneous Network Activity and Synaptic Development.

Authors:  Daniel Kerschensteiner
Journal:  Neuroscientist       Date:  2013-11-25       Impact factor: 7.519

10.  LTD and LTP at the developing retinogeniculate synapse.

Authors:  Jokūbas Ziburkus; Emily K Dilger; Fu-Sun Lo; William Guido
Journal:  J Neurophysiol       Date:  2009-09-23       Impact factor: 2.714

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