Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium

M. S. Jensen, R. Azouz, Y. Yaari

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Abstract

1. The distribution of distinctive firing modes within the population of CA1 pyramidal cells and their modulation by the extracellular concentration of potassium ([K+](o)) were investigated with intracellular recordings in rat hippocampal slices. 2. Pyramidal cells were injected with long (>250 ms) and brief (3-5 ms) positive current pulses of increasing intensity. In normal [K+](o) (3.5 mM), most cells (38 of 46 cells; 83%) were regular spiking neurons (generating accommodating trains of independent action potentials during long depolarizations and a single spike in response to brief stimuli). The remaining pyramidal cells (8 of 46; 17%) displayed differential tendencies to generate stereotyped clusters of action potentials, or burst, according to which they were grouped into three subsets of endogenous bursters: grade I, bursting only when stimulated with long depolarizing current pulses (6 of 46; 13%); grade II, bursting also in response to brief stimulation (1 of 46; 2%); grade III, bursting also spontaneously even in absence of synaptic transmission (1 of 46; 2%). 3. Raising [K+](o) from 3.5 to 7.5 mM (high [K+](o)) significantly reduced resting membrane potential and input impedance but did not change the threshold potential for eliciting an action potential. 4. Raising [K+](o) to 7.5 mM reversibly converted many regular spiking cells to bursters. Likewise, the burst tendency of normally bursting pyramidal cells increased to a higher grade in high [K+](o). Consequently, the fraction of bursters in high [K+](o) (17 of 41 cells; 42%) was ~2.5-fold higher than in normal [K+](o) and their differential distribution was shifted toward higher grades of bursting. In this condition, 15% (6 of 41) of the pyramidal cells were grade I, 17% (7 of 41) were grade II, and 10% (4 of 41) were grade III bursters. There were no significant differences in resting membrane potential, input resistance, spike threshold, or spike amplitude between the four subsets of pyramidal cells. 5. The fast repolarization phase of solitary action potentials terminated at slightly depolarized potentials and was followed by a slow after depolarization (ADP). The ADP in 50% of the cells (n = 20) was 'active,' i.e., membrane potential redepolarized during the ADP. When measured from the same baseline potential, ADP amplitudes were enhanced by raising [K+](o). Mostly neurons with active ADP became bursters in high [K+](o). 6. We conclude that the firing patterns of CA1 pyramidal cells form a continuum of variation in 'burstiness' that ranges from regular spiking to spontaneous burst firing. Raising [K+](o) shifts the distribution of firing patterns along this continuum toward increased burstiness by enhancing an endogenous burst mechanism that is primordially expressed in active ADPs.

Original languageEnglish
Pages (from-to)831-839
Number of pages9
JournalJournal of Neurophysiology
Volume71
Issue number3
DOIs
StatePublished - 1 Jan 1994
Externally publishedYes

ASJC Scopus subject areas

  • Neuroscience (all)
  • Physiology

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