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The Journal of Neuroscience, May 15, 1998, 18(10):3919-3928
Dendritic Spikes Are Enhanced by Cooperative Network Activity in
the Intact Hippocampus
Anita
Kamondi,
László
Acsády, and
György
Buzsáki
Center for Molecular and Behavioral Neuroscience, Rutgers, The
State University of New Jersey, Newark, New Jersey 07102
In vitro experiments suggest that dendritic fast
action potentials may influence the efficacy of concurrently active
synapses by enhancing Ca2+ influx into the
dendrites. However, the exact circumstances leading to these effects in
the intact brain are not known. We have addressed these issues by
performing intracellular sharp electrode recordings from
morphologically identified sites in the apical dendrites of CA1
pyramidal neurons in vivo while simultaneously
monitoring extracellular population activity. The amplitude of
spontaneous fast action potentials in dendrites decreased as a function
of distance from the soma, suggesting that dendritic propagation of
fast action potentials is strongly attenuated in vivo.
Whereas the amplitude variability of somatic action potentials was very small, the amplitude of fast spikes varied substantially in distal dendrites. Large-amplitude fast spikes in dendrites occurred during population discharges of CA3-CA1 neurons concurrent with field sharp
waves. The large-amplitude fast spikes were associated with bursts of
smaller-amplitude action potentials and putative
Ca2+ spikes. Both current pulse-evoked and
spontaneously occurring Ca2+ spikes were always
preceded by large-amplitude fast spikes. More spikes were observed in
the dendrites during sharp waves than in the soma, suggesting that
local dendritic spikes may be generated during this behaviorally
relevant population pattern. Because not all dendritic spikes produce
somatic action potentials, they may be functionally distinct from
action potentials that signal via the axon.
Key words:
plasticity; calcium spikes; long-term potentiation; spike
propagation; signaling; action potentials
Copyright © 1998 Society for Neuroscience 0270-6474/98/18103919-10$05.00/0
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[Full Text]
[PDF]
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