Re-analysis of the antidromic cortical response. II. On the contribution of cell discharge and PSPs to the evoked potentials

Abstract

Simultaneous recordings were obtained from single pyramidal tract (PT) neurons and from the surface of the motor cortex following stimulation of the surgically isolated PT of barbiturate-anesthetized cats. In agreement with previous suggestions (Humphrey 1968), the discharge of the PT cell population was found to contribute negligibly to a cortical surface record, whereas recurrent IPSPs gave rise to a comparatively large amplitude (0.4-0.7 mV) surface negativity. The results appeared to provide particularly clea evidence in favor of the hypotheses advanced by Eccles (1951) and by Purpura (1959) (i.e., that cortical gross waves derive largely from PSPs), because in this instance cell discharge and PSPs were separable in time, allowing the contributions of each to be independently assessed. However, the usual explanations advanced to account for such differential contribution (temporal and spatial dispersion of unit responses, cancellation of potential fields generated by responses of opposite polarity, etc.) appeared inadequate, suggesting that an additional, perhaps more fundamental mechanism was involved. To pursue this possibility, mathematical theories of electrotonic and volume conduction were used to calculate the extracellular potentials generated by a spike and a long duration IPSP in a pyramidally shaped model neuron. The results indicated that in generating a potential at a distant extracellular point (more than 150-200 μ from the active membrane regions), a pyramidally shaped neuron may behave essentially as a "low-pass filter"; i.e., long duration intracellular potentials may give rise to a greater external voltage than do short duration transients of even larger amplitude. The biophysical properties of the cell that might be responsible for this result were discussed. A population of model cells was then constructed, on the basis of experimental data concerning the distribution of evoked PT unit activity over time and cortical depth. The theoretical potentials distributions generated by the model population agreed well with those experimentally observed during the discharge of, and IPSPs within, the PT cell population. Possible implications of the model for interpretations of cortical gross potential data were discussed. © 1968.