INTRODUCTION
In recent years physiologists have become quite adept at probing into neurons with intracellular microelectrodes. They are now able, in fact, to measure (a) the voltage change across the postsynaptic membrane elicited by a single presynaptic impulse (see, for examples, references [1] and [2]) and (b) the voltage-current characteristics across a localized region of the nerve cell membrane [(3)], [(4)], [(5)], [(6)]. With microelectrodes, physiologists have been able to examine not only the all-or-none spike generating and propagating properties of axons but also the electrical properties of somatic and dendritic structures in individual neurons. The resulting observations have led many physiologists to believe that the individual nerve cell is a potentially complex information-processing system far removed from the simple two-state device envisioned by many early modelers. This new concept of the neuron is well summarized by Bullock in his 1959 Science article [(10)]. In the light of recent physiological literature, one cannot justifiably omit the diverse forms of somatic and dendritic behavior when assessing the information-processing capabilities of single neurons. This is true regardless of the means of assessment—whether one uses mathematical idealizations, electrochemical models, or electronic analogs. We have been interested specifically in electronic analogs of the neuron; and in view of the widely diversified behavior which we must simulate, our first goal has been to find a unifying concept about which to design our analogs. We believe we have found such a concept in the Modern Ionic Hypothesis, and in this paper we will discuss an electronic analog of the neuron which was based on this hypothesis and which simulated not only the properties of the axon but also the various subthreshold properties of the somata and dendrites of neurons.
We begin with a brief summary of the various types of subthreshold activity which have been observed in the somatic and dendritic structures of neurons. This is followed by a brief discussion of the Hodgkin-Huxley data and of the Modern Ionic Hypothesis. An electronic analog based on the Hodgkin-Huxley data is then introduced, and we show how this analog can be used to provide all of the various types of somatic and dendritic activity.
SUBTHRESHOLD ELECTRICAL ACTIVITY
IN NEURONS
In studying the recent literature in neurophysiology, one is immediately struck by the diversity in form of both elicited and spontaneous electrical activity in the single nerve cell. This applies not only to the temporal patterns of all-or-none action potentials but also to the graded somatic and dendritic potentials. The synaptic membrane of a neuron, for example, is often found to be electrically inexcitable and thus incapable of producing an action potential; yet the graded, synaptically induced potentials show an amazing diversity in form. In response to a presynaptic impulse, the postsynaptic membrane may become hyperpolarized (inhibitory postsynaptic potential), depolarized (excitatory postsynaptic potential), or remain at the resting potential but with an increased permeability to certain ions (a form of inhibition). The form of the postsynaptic potential in response to an isolated presynaptic spike may vary from synapse to synapse in several ways, as shown in [Figure 1]. Following a presynaptic spike, the postsynaptic potential typically rises with some delay to a peak value and then falls back toward the equilibrium or resting potential. Three potentially important factors are the delay time (synaptic delay), the peak amplitude (spatial weighting of synapse), and the rate of fall toward the equilibrium potential (temporal weighting of synapse). The responses of a synapse to individual spikes in a volley may be progressively enhanced (facilitation), diminished (antifacilitation), or neither [(1)], [(2)], [(7)], [(8)]. Facilitation may be in the form of progressively increased peak amplitude, or in the form of progressively decreased rate of fall ([see Figure 2]). The time course and magnitude of facilitation or antifacilitation may very well be important synaptic parameters. In addition, the postsynaptic membrane sometimes exhibits excitatory or inhibitory aftereffects (or both) on cessation of a volley of presynaptic spikes [(2)], [(7)]; and the time course and magnitude of the aftereffects may be important parameters. Clearly, even if one considers the synaptic potentials alone, he is faced with an impressive variety of responses. Examples of the various types of postsynaptic responses may be found in the literature, but for purposes of the present discussion the idealized wave forms in [Figure 2] will demonstrate the diversity of electrical behavior with which one is faced.
Figure 1—Excitatory postsynaptic potentials in response to a single presynaptic spike