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Do neurons have a voltage or a current threshold for action potential initiation?

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Abstract

The majority of neural network models consider the output of single neurons to be a continuous, positive, and saturating firing ratef(t), while a minority treat neuronal output as a series of delta pulses ∑δ (t — t i ). We here argue that the issue of the proper output representation relates to the biophysics of the cells in question and, in particular, to whether initiation of somatic action potentials occurs when a certain thresholdvoltage or a thresholdcurrent is exceeded. We approach this issue using numerical simulations of the electrical behavior of a layer 5 pyramidal cell from cat visual cortex. The dendritic tree is passive while the cell body includes eight voltage- and calcium-dependent membrane conductances.

We compute both the steady-state (I static∞ (V m )) and the instantaneous (I o (Vm)) I–V relationships and argue that the amplitude of the local maximum inI static∞ (V m ) corresponds to the current thresholdI th for sustained inputs, while the location of the middle zero-crossing ofI o corresponds to a fixed voltage thresholdV th for rapid inputs. We confirm this using numerical simulations: for “rapid” synaptic inputs, spikes are initiated if the somatic potential exceedsV th, while for slowly varying inputI th must be exceeded. Due to the presence of the large dendritic tree, no charge thresholdQ th exists for physiological input.

Introducing the temporal average of the somatic membrane potential 〈(V m)〉 while the cell is spiking repetitively, allows us to define a dynamic I-V relationship dynamic∞ (〈(V m)〉). We find an exponential relationship between 〈(V m)〉 and the net current sunk by the somatic membrane during spiking (diode-like behavior). The slope ofI∞/dynamic(〈(V m))〉 allows us to define a dynamic input conductance and a time constant that characterizes how rapidly the cell changes its output firing frequency in response to a change in its input.

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Authors and Affiliations

  1. Computation and Neural Systems Program, 139-74, California Institute of Technology, 91125, Pasadena, CA, US

    Christof Koch & Öjvind Bernander

  2. Computation and Neural Systems Program, 139-74, California Institute of Technology, 91125, Pasadena, CA, US

    Rodney J. Douglas

  3. MRC Anatomical Neuropharmacology Unit, OX1 3TH, Oxford, UK

    Rodney J. Douglas

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  2. Öjvind Bernander
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Koch, C., Bernander, Ö. & Douglas, R.J. Do neurons have a voltage or a current threshold for action potential initiation?. J Comput Neurosci 2, 63–82 (1995). https://doi.org/10.1007/BF00962708

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