Single-channel currents trigger action potentials insmall cultured hippocampal neurons.

Abstract

Spontaneous neuronal impulse activity appears to play a key role in some neural processes, such as the normal establishment of interneuronal connections during development. In addition, spontaneous impulses may be essential for the functional operation of neuronal networks. Mechanisms of spontaneous non-pacemaker impulse generation are, however, not well known. In this work, spontaneous electrical activity in small cultured hippocampal neurons from rat was studied with tight-seal recording techniques. The results demonstrate that spontaneous individual openings of single ion channels can trigger impulse generation in these highresistance cells. First, impulses recorded in the whole-cell mode were apparently induced by spontaneous plateau-potential events showing the characteristics expected from individual openings and closures of ion channels. Second, patch-clamp recordings in the cell-attached configuration showed that openings of single ion channels in the patch membrane could trigger cellular impulses, detected as biphasic current deflections. These flndings suggest that the random gating of ion channel molecules can be used as a mechanism for stochastic triggering of spontaneous impulses in mammalian central neurons.Several neuronal cell types are capable of spontaneously generating electrical impulses in the absence of synaptic input or other external stimuli (1, 2). Some of these neuron types, as well as heart cells, can fire repetitive impulses with remarkably regular intervals. The mechanisms of such regular spontaneous activity have been extensively studied (3,4). In other cells, impulses can be generated at random time intervals (5). Impulses of such stochastic nature may be critical for neural function. Impulses originating at random are, for instance, thought to play a crucial role for the normal establishment of synaptic connections during development (6). Furthermore, theoretical work shows that random signaling may contribute essentially to the informationprocessing capabilities of neuronal networks (7-9). In spite of this, the mechanisms underlying random initiation of impulses are not well known.A possible mechanism for achieving randomly induced impulses is to use the random nature of ion channel kinetics. This is possible if the random openings or closures of a small number of ion channels can trigger impulses. A small number of channels is needed for randomness, to avoid the averaging effect of large populations of channels. Several reports have been presented indicating that current events originating from single ion channels may induce impulses in some secretory cell types (10-12) and in olfactory receptor cells (13)(14)(15).In this study, we present evidence suggesting that individual openings or closures of single ion channels can induce impulses in mammalian central neurons. The evidence was obtained by tight-seal recordings from a subpopulation of small cultured neurons from rat hippocampus. These cells have a high input resistance (several gigaohms) and a very low current thre...

On the Possibility of Universal Neural Coding of Subjective Experience

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“…interesting features, such as graded action potentials (Johansson et al, 1992), spontaneous activity induced by single channel openings (Johansson and Å rhem, 1994), and the capability of functioning as a memory device (Johansson et al, 1995). The figure shows the activity of model neurons with different densities of Na and K channels, reflecting the effect of selectively blocking Na and K channels in a state-independent manner.…”