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PMID: 10212317 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Retinal waves are governed by collective network properties.

Butts DA, Feller MB, Shatz CJ, Rokhsar DS

Abstract

Propagating neural activity in the developing mammalian retina is required for the normal patterning of retinothalamic connections. This activity exhibits a complex spatiotemporal pattern of initiation, propagation, and termination. Here, we discuss the behavior of a model of the developing retina using a combination of simulation and analytic calculation. Our model produces spatially and temporally restricted waves without requiring inhibition, consistent with the early depolarizing action of neurotransmitters in the retina. We find that highly correlated, temporally regular, and spatially restricted activity occurs over a range of network parameters; this ensures that such spatiotemporal patterns can be produced robustly by immature neural networks in which synaptic transmission by individual neurons may be unreliable. Wider variation of these parameters, however, results in several different regimes of wave behavior. We also present evidence that wave properties are locally determined by a single variable, the fraction of recruitable (i.e., nonrefractory) cells within the dendritic field of a retinal neuron. From this perspective, a given local area's ability to support waves with a wide range of propagation velocities-as observed in experiment-reflects the variability in the local state of excitability of that area. This prediction is supported by whole-cell voltage-clamp recordings, which measure significant wave-to-wave variability in the amount of synaptic input a cell receives when it participates in a wave. This approach to describing the developing retina provides unique insight into how the organization of a neural circuit can lead to the generation of complex correlated activity patterns.

MeSH Terms
Animals Computer Simulation Dendrites/physiology Image Processing, Computer-Assisted Mammals Models, Neurological Nerve Net/physiology Neurons/physiology Neurotransmitter Agents/physiology Retina/cytology,physiology Retinal Ganglion Cells/physiology Synaptic Transmission
Chemicals
Neurotransmitter Agents
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Butts D A
Physical Biosciences Division, Lawrence Berkeley National Laboratory, and the Department of Physics, University of California, Berkeley, California 94720-7300, USA. [email protected]
Feller M B
Shatz C J
Rokhsar D S
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1999-05-01
Pages
3580-93
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782231
Subset
IM
Grants
NIMH NIH HHS · MH 48108 · United States
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