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Journal of Neuroscience, Vol 14, 1060-1078, Copyright © 1994 by Society for Neuroscience
Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro
ME Dailey, J Buchanan, DE Bergles and SJ Smith
Department of Molecular and Cellular Physiology, Stanford University School of Medicine, California 94305-5426.
Hippocampal slices from early postnatal rat were used to study mossy fiber
(MF) growth and synaptogenesis. The ability of MFs to form new giant
synapses within isolated tissue slices was established by a series of
experiments involving synapsin I immunohistochemistry, electron microscopy,
and whole-cell recordings. When hippocampal slices from immature rats were
cultured for up to 2 weeks, the distribution of giant MF terminals was
similar to that found in vivo. Using a lesioning procedure, we determined
that MFs in slices extend and form appropriate synaptic connections with
normal target CA3 pyramidal cells. MF terminals were dispersed more widely
than normal within the CA3 pyramidal layer after a lesion, but electron
microscopy indicated that synaptic junctions were still primarily
associated with pyramidal cell dendrites and not the somata. Establishment
of functional synaptic input in vitro was confirmed by whole-cell
recordings of MF-driven excitatory postsynaptic currents (50 pA to 1 nA) in
pyramidal cells. The results establish for the first time that an MF
projection with appropriate and functional synaptic connections can be
formed de novo and not just maintained in excised hippocampal slices. The
cellular dynamics underlying MF growth and synaptogenesis were examined
directly by time-lapse confocal imaging of fibers selectively stained with
a fluorescent membrane dye (Dil or DiO). MFs growing deep within isolated
tissue slices were tipped by small (5-10 microns), active growth cones that
advanced at variable rates (5-25 microns/hr). Furthermore, dynamic
filopodial structures were seen at small varicosities along the length of
developing MFs, which may identify nascent en passant synaptic contacts.
The hippocampal slice preparations are shown to support normal development
of MF connections and allow for direct visualization of the cellular
dynamics of synapse formation in a mammalian CNS tissue environment.
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