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Journal of Neuroscience, Vol 10, 2601-2613, Copyright © 1990 by Society for Neuroscience
Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex
E Friauf, SK McConnell and CJ Shatz
Department of Neurobiology, Stanford University School of Medicine, California 94305.
Among the first postmitotic cells of the cerebral cortex is a special
population located below the cortical plate: the subplate neurons. These
neurons reach a high degree of morphological maturity during fetal life,
well before the neurons of the cortical layers have matured, yet nearly all
of these cells die after birth in the cat. Subplate neurons are also known
to receive synaptic contacts. Here we have investigated whether these
contacts are functional by making intracellular recordings from subplate
neurons in cortical slices maintained in vitro. Subplate neurons were
identified based on their location and morphology by injecting them with
biocytin following the intracellular recordings. At all ages studied
between embryonic day 50 and postnatal day 9, electrical stimulation of the
optic radiations elicited EPSPs and synaptic and antidromic spikes in
subplate neurons, indicating that some of the synapses seen at the
ultrastructural level are indeed capable of synaptic transmission. The
spiking patterns of 39 morphologically identified subplate neurons were
examined by injecting depolarizing current, which revealed that a large
majority gave only a single spike or a brief train of spikes in response to
maintained depolarization, in contrast to the regular spiking pattern found
in many neurons of adult cortex. Biocytin injections into subplate neurons
revealed that they are a morphologically heterogeneous population with
respect to their dendritic branching patterns; roughly half were inverted
pyramids, the classic subplate neuron morphology. The axonal processes of
subplate neurons were remarkable in that many not only arborized within the
subplate, but also entered the cortical plate and terminated in the
marginal zone. At early postnatal ages, these axons also gave off
collaterals within cortical layer 4. The results of this study indicate
that subplate neurons participate in synaptic microcircuits during
development. While the presynaptic identity of the input to subplate
neurons is not known conclusively, it is likely that geniculocortical
axons, which wait in close proximity to subplate neurons, contribute
significantly. The pattern of axonal branching of subplate neurons also
implies that information conferred to subplate neurons may be relayed, in
turn, to the neurons of cortical layer 4. Finally with the death of
subplate neurons, the geniculocortical axons leave the subplate and invade
the cortical plate to innervate directly the neurons of layer 4. Thus,
subplate neurons may function as a crucial, but transient synaptic link
between waiting geniculocortical axons and their ultimate target cells in
the cortex.
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