Active dissociation of intracortical spiking and high gamma activity

Cortical high gamma-band activity (HGA) is used in many scientific investigations^1-18, yet its biophysical source is a matter of debate. Two leading hypotheses are that HGA predominantly represents summed postsynaptic potentials or-more commonly-that it predominantly represents summed local spikes. If the latter were true, the nearest neurons to an electrode should contribute most to HGA recorded on that electrode. To test these hypotheses, here we trained monkeys (Macaca mulatta) to decouple local spiking from HGA on a single electrode using a brain-machine interface. Their ability to decouple them suggested that HGA is probably not generated simply by summed local spiking. Instead, HGA correlated with co-firing of neuronal populations that were widely distributed across millimetres of cortex. The neuronal spikes that contributed more to this co-firing also contributed more to, and preceded, spike-triggered HGA. These results suggest that HGA arises mainly from summed postsynaptic potentials triggered by the synchronous co-firing of widely distributed neurons.