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Journal of Neuroscience, Vol 10, 3664-3684, Copyright © 1990 by Society for Neuroscience
Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells
WM Roberts, RA Jacobs and AJ Hudspeth
Institute of Neuroscience, University of Oregon, Eugene 97403.
Calcium ions serve as intracellular messengers in 2 activities of hair
cells: in conjunction with Ca2(+)-activated K+ channels, they produce the
electrical resonance that tunes each cell to a specific frequency of
stimulation, and they trigger the release of a chemical synaptic
transmitter. Our experiments indicate that both of these functions are
conducted within a region that extends a few hundred nanometers around each
presynaptic active zone. In focal electrical recordings from the plasma
membranes of isolated anuran hair cells, we found nearly all of a cell's
Ca2+ channels and Ca2(+)-activated K+ channels clumped at a fixed ratio in
an average of 20 clusters on the basolateral membrane surface. Because
serial-section electron microscopy indicated that each hair cell has
approximately 19 afferent synaptic contacts with a similar distribution
upon its basolateral surface, we conclude that the channel clusters
coincide with synaptic active zones. Ensemble-variance analysis of current
fluctuations indicated that each cell has a total of approximately 1800
Ca2+ channels and approximately 700 Ca2(+)- activated K+ channels; if these
are uniformly divided, we estimate that each channel cluster contains
approximately 90 Ca2+ and approximately 40 Ca2(+)-activated K+ channels.
Freeze-fracture electron microscopy demonstrated an average of 133 large
intramembrane particles in the presynaptic membrane at each active zone, an
observation that suggests that the particles are the clustered channels. We
used the K+ channel's sensitivity to intracellular Ca2+ to assay the
concentration of free Ca2+ in the presynaptic cytoplasm, which we found to
vary between 10 microM and 1 mM over the physiological range of membrane
potentials. The inferred concentrations agreed with the values predicted
for free diffusion of Ca2+ away from Ca2+ channels scattered randomly
within a 300-nm-diameter synaptic active zone. The close association among
Ca2+ channels, Ca2(+)-activated K+ channels, and synaptic active zones is
necessary both for the rapid activation of K+ currents required in
electrical resonance and for the transmission at afferent synapses of
information about the phases of high-frequency stimuli.
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