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The Journal of Neuroscience, May 1, 1999, 19(9):3580-3593
Retinal Waves Are Governed by Collective Network Properties
Daniel A.
Butts1,
Marla
B.
Feller2, 3,
Carla J.
Shatz2, and
Daniel S.
Rokhsar1
1 Physical Biosciences Division, Lawrence Berkeley
National Laboratory, and the Department of Physics, University of
California, Berkeley, California 94720-7300, 2 Howard
Hughes Medical Institute and the Department of Molecular and Cell
Biology, University of California, Berkeley, California 94720-3200, and
3 National Institutes of Health, National Institute of Neurological
Disorders and Stoke, Bethesda, Maryland 20892-4156
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 experimentreflects 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.
Key words:
visual system; development; calcium waves; model; developing retina; correlated activity
Copyright © 1999 Society for Neuroscience 0270-6474/99/1993580-14$05.00/0
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