Anatomical and molecular biological observations suggest
that the brain is in a perpetual state of change. In contrast
to this change of the substrate is our subjective experience
of certain constancy of our biographical data and skills
we acquired. I suggest that constancy can be maintained
in the ever- changing anatomical substrate by rehearsal
or repetition. Reuse of the network storing information
can occur consciously or while we are asleep. To address
this issue we examined how the long-term firing rates and
patterns of pyramidal cells are maintained and regulated
in different behavioral states. In a familiar environment,
the discharge frequency of simultaneously recorded individual
CAI pyramidal neurons and the coactivation of cell pairs
remained highly correlated across sleep-wake- sleep sequences
in rats. However, both measures were affected when new sets
of neurons were activated in a novel environment. Nevertheless,
the grand mean firing rate of the whole pyramidal cell population
remained constant across behavioral states and testing conditions.
The findings suggest that long-term firing patterns of single
cells can be modified by experience. We hypothesize that
increased firing rates of recently used neurons are associated
with a concomitant decrease in the discharge activity of
the remaining population, leaving the mean excitability
of the hippocampal network unaltered. Next we discuss the
physiological basis of this homeostatic process.
Pyramidal neurons fire not only single spikes but also
bursts of spikes. Other investigators suggested that bursts
are particularly important in the induction of synaptic
plasticity. However, the conditions necessary for burst
induction are not known. CAl pyramidal cell burst activity
was examined in behaving rats. The fraction of bursts was
not reliably higher in place field centers, but rather in
places where discharge frequency was 6-7 Hz (theta oscillation
frequency). Burst probability was lower, and bursts were
shorter, after recent spiking activity than after prolonged
periods of silence (100ms- Is). Burst initiation probability
and burst length were correlated with extracellular spike
amplitude and with intracellular action potential rising
slope, indicating that intrinsic properties of the neurons
are responsible for the "competition" between single spikes
and complex spike bursts. Thus, single spikes triggered
by a weak afferent input may suppress the later induction
of a burst by a strong input. Thus, the subthreshold or
suprathreshold nature of one input determines whether another
(strong) input produces a burst or not. Given the suggested
importance of burst discharges in synaptic plasticity, our
observations provide some interesting possibilities for
the regulation of discharge rate in pyramidal neurons.
Several findings support the importance of the temporal
order of presynaptic and postsynaptic activity in neuronal
plasticity: a weak input, eliciting an EPSP, followed by
a strong, burst-inducing input is a necessary and sufficient
condition for strengthening the weak input (Hebbian rule).
The shorter the time interval between the weak and strong
input, the larger the magnitude of synaptic potentiation.
Conversely, reversing the temporal order of the weak and
strong can lead to depression of the weak input or depotentiating
its previously gained weight increase.
Given the Hebbian rule, we propose that bursts may be conceived
as a homeostatic mechanism to maintain synaptic strength.
Once the weak input becomes suprathreshold, the consequent
reduction of Na, channel availability as a result of the
action potential will reduce the ability of strong inputs
to induce a burst. The shorter the time between the weak
(but now suprathreshold) and strong inputs, the stronger
the "veto effect" of the single spike. Should the strength
of the synapse decay with time or get depotentiated actively,
the weak synaptic input may become subthreshold again. At
this point the strong input becomes instantly effective
in inducing a burst, which can then potentiate the weakened
synapse. In essence, I propose that the veto effect of single
spikes on burst probability is a potential mechanism for
regulating synaptic strength. The proposed homeostatic mechanism
is operative in a single cell and depends primarily on the
immediate spiking history of the neuron.
