EEG oscillations at 600 Hz are macroscopic markers for cortical spike bursts

Abstract

The human electroencephalogram (EEG) is generated predominantly by synchronised cortical excitatory postsynaptic potentials oscillating at frequencies <100 Hz. Unusually, EEG responses to electrical nerve stimulation contain brief bursts of high-frequency (600 Hz) wavelets. Here we show, in awake monkeys, that a subset of primary somatosensory cortex single units consistently fires both bursts and single spikes phase-locked to EEG wavelets. Spike bursts were also evoked by tactile stimuli, proving that this is a natural response mode. EEG wavelets at 600 Hz may therefore permit non-invasive assessment of population spike timing in human cortex.

Figure 1. Example of recordings of epidural EEG and single-unit responses to median nerve stimulation

A, schematic of the experimental arrangement. B, average of epidural EEG triggered by median nerve stimulation (n = 1298), using a wideband filter setting (3 Hz to 2 kHz). C, the corresponding high-pass filtered average (428 Hz to 2 kHz). D, example single sweep responses of an S1 neuron. E, distribution of the number of response spikes per stimulus for this cell. F, peristimulus time histogram (n = 1298 stimuli). The grey-shaded region marks the period used to count the number of response spikes per stimulus, illustrated in E. G, inter-spike interval histogram. Arrows in B–D mark the time of stimulus delivery.

Figure 2. Correspondence of single-unit responses with epidural averages

A, thick lines show summed peri-stimulus time histograms (PSTHs) over all units recorded in each animal (n = 17 units for monkey 33; n = 15 for monkey 32. Mean number of stimuli given per unit was 1128, range 150-2192). PSTHs have been normalised by dividing by the number of stimuli before addition in order to weight each neuron equally. Thin lines show a representative average of the epidural EEG (n = 1298 stimuli, monkey 33; n = 782 stimuli, monkey 32). Arrowheads mark the time of median nerve stimulation. B, the results of high-pass filtering the traces in A (>428 Hz).

Figure 3. Example of burst responses to natural tactile stimuli

A, the location of the cutaneous receptive field of the cell illustrated in Fig. 1. B, single-sweep responses of this cell to tap stimuli given to this region of skin using a stylus. Arrow marks the time of skin contact. C, distribution of the number of response spikes per stimulus. D, inter-spike interval histogram. E, peri-stimulus time histogram (n = 496 tap stimuli). The grey-shaded region indicates the period over which the number of response spikes was measured for C.

Figure 4. Single response spikes occur at preferred latencies after the stimulus

A, single-sweep responses of a neuron from monkey 32, which fired only one spike per stimulus in response to median nerve stimulation (arrow). B, peri-stimulus time histogram (PSTH), showing a bimodal distribution of response latencies. C, high-pass filtered summed PSTH of 17 cells that responded to nerve stimulation with only a single spike (thick line). This is overlain on a high-pass filtered average of the epidural EEG.