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Journal of Neuroscience, Vol 13, 313-323, Copyright © 1993 by Society for Neuroscience
Prenatal development of excitability in cat retinal ganglion cells: action potentials and sodium currents
I Skaliora, RP Scobey and LM Chalupa
Department of Psychology, University of California, Davis 95616.
The development of precise retinofugal projections is dependent on
activity-mediated events, but as yet nothing is known about the ontogeny of
excitable membrane properties in retinal ganglion cells (RGCs). In order to
begin to understand how functional maturity is attained in these neurons,
whole-cell patch-clamp recordings were obtained from acutely dissociated
RGCs of fetal and postnatal timed- pregnant cats. Current-clamp recordings
revealed a pronounced developmental increase in the proportion of RGCs
capable of generating action potentials. At embryonic day 30 (E30), 5 weeks
before birth and during a time when RGCs are still being generated,
electrical stimulation elicited spikes in only a third of the cells. None
of these neurons were capable of multiple discharges in response to
maintained depolarization. The proportion of spiking neurons increased
during ontogeny, such that by E55 all RGCs could be induced to generate
action potentials, with the majority manifesting repetitive spiking
patterns. Application of tetrodotoxin abolished spike activity of all fetal
RGCs, indicating that sodium-mediated action potentials are present very
early in development. At the same time, voltage-clamp recordings revealed
significant ontogenetic modifications in several key properties of the
sodium currents (INa). These were (1) a twofold increase in Na current
densities; (2) a shift in the voltage dependence of both activation and
steady state inactivation: with maturity, sodium currents activate at more
negative potentials, while steady state inactivation of INa occurs at less
negative potentials; and (3) a decrease in decay time constants of the Na
current, at membrane potentials negative to -15 mV. These developmental
changes were largely restricted to the period of axon ingrowth (E30-E38),
suggesting that maturation of INa is not the limiting factor for the onset
of activity- dependent restructuring of retinofugal projections.
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