Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons

Alexander Reyes, E. E. Fetz

Research output: Contribution to journalArticle

Abstract

1. The effects of small, brief depolarizing pulses and excitatory postsynaptic potentials (EPSPs) on neuronal firing were examined in layer V neurons in slices of cat sensorimotor cortex. During intracellular recording, brief depolarizing current pulses (duration, 0.5-2.0 ms; amplitude, 0.1-4.0 nA) were injected in neurons to produce pulse potentials (PPs) with a near- linear rise to a peak (0.08-3.6 mV; rise time = pulse duration) followed by an exponential decay. These PPs resembled EPSPs evoked by electrical stimulation of adjacent sites. When injected in neurons that were induced to discharge tonically, the PPs shortened the interspike intervals (ISIs) in two ways, depending on their time of arrival in the ISI. 2. Toward the end of the ISI, the PPs crossed a time-varying firing level, thereby directly evoking action potentials and shortening the ISIs. These directly evoked spikes occurred during the rise or peak of the PPs. The absolute firing level increased with the membrane trajectory during the latter part of the ISI. 3. PPs that appeared earlier in the ISI did not cross firing level directly but could nevertheless shorten the ISI by a slow regenerative process. The indirectly evoked spikes occurred after the peak of the PPs, at latencies whose magnitude and variability increased as the PPs appeared at successively earlier times in the ISI. PPs that occurred during the initial portion (approximately the 1st 3rd) of the ISI did not affect ISI duration. 4. Stimulus-evoked EPSPs shortened the ISIs in a manner similar to that of PPs. Like PPs, EPSPs caused direct crossings late in the ISI and indirect crossings earlier. Comparison of the mean and maximum ISI shortenings and the range of delays in which the PPs and EPSPs consistently produced ISI shortenings revealed no systematic differences. These similarities suggest that PPs may be used to simulate the ISI shortenings caused by EPSPs. 5. To characterize possible mechanisms underlying the ISI shortening, we examined the PP shapes at different times in the ISI. PPs immediately following a spike were smaller and decayed more rapidly than those evoked by the same current at rest. Late in the ISI, when the membrane potential was >5 mV above rest, the PP height exceeded that of the PP at rest. This amplitude increase may be due to activation of the persistent sodium current. 6. PPs appearing at intermediate times in the ISI activated a slow regenerative process, causing a stereotyped, near-exponential rise in the membrane trajectory that crossed firing level after ~3.1 ± 1.6 (SD) ms. Threshold for this process was 4.3 ± 2.4 mV below firing level. 7. The combination of the time-varying firing level and the slow regenerative process allowed most of the voltage transients to shorten the ISI and thereby increase the firing rate of the cortical neurons.

Original languageEnglish (US)
Pages (from-to)1661-1672
Number of pages12
JournalJournal of Neurophysiology
Volume69
Issue number5
StatePublished - 1993

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Excitatory Postsynaptic Potentials
Cats
Neurons
Membranes
Membrane Potentials
Electric Stimulation
Action Potentials
Sodium

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

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Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. / Reyes, Alexander; Fetz, E. E.

In: Journal of Neurophysiology, Vol. 69, No. 5, 1993, p. 1661-1672.

Research output: Contribution to journalArticle

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