Measurement of the extraocular spike potential during saccade countermanding

Abstract

The stop signal task is used to investigate motor inhibition. Several groups have reported partial electromyogram (EMG) activation when subjects successfully withhold manual responses and have used this finding to define the nature of response inhibition properties in the spinal motor system. It is unknown whether subthreshold EMG activation from extraocular muscles can be detected in the saccadic response version of the stop signal task. The saccadic spike potential provides a way to examine extraocular EMG activation associated with eye movements in electroencephalogram (EEG) recordings. We used several techniques to isolate extraocular EMG activation from anterior electrode locations of EEG recorded from macaque monkeys. Robust EMG activation was present when eye movements were made, but no activation was detected when saccades were deemed canceled. This work highlights a key difference between the spinal motor system and the saccade system.

Fig. 1.

The stop signal (or countermanding) task in a schematic representation. No-stop trials (top) were initiated when monkeys fixated a centrally presented fixation point. After a variable time, the fixation point was extinguished and simultaneously a peripheral target was presented at one of two possible locations. Monkeys were required to fixate targets with quick saccades for juice rewards. Stop trials (bottom) were initiated in the same way. After a variable time, termed the stop signal delay (SSD), the fixation point was reilluminated, instructing the monkeys to withhold movement. Successful inhibition of saccades resulted in a reward (canceled trials), but errant saccades resulted in no reward (noncanceled trials). The solid squares indicate stimulus locations. Dotted circles represent the area of fixation. F, fixation point; T, target; RT, reaction time.

Fig. 2.

The timing of eye movements relative to task events was displayed using event-related velocity (ERV) plots. This technique is similar to creating event-related potentials (ERPs) from raw electroencephalogram (EEG) signals. Top left: single trial radial positions for a sample session aligned on the saccade onset. Bottom left: instantaneous radial velocity for the same trials (black) along with the mean instantaneous velocity collapsed across all trials (red). Top right: same single trial radial positions in relation to the target onset. Bottom right: single trial instantaneous velocity in relation to the target onset as well as the average radial velocity collapsed across all trials. This target-aligned ERV gives information about the average saccade latency, velocity, and duration relative to the target onset.

Fig. 3.

Saccade dynamics do not differ between no-stop and noncanceled trials. The scatterplots show saccade amplitude versus peak saccade velocity (main sequences) across all sessions. The histograms display associated probability densities for each measurement. Bin widths are 10°/s for velocity distributions and 0.25° for amplitude distributions. Blue dots and dashed lines represent saccades on no-stop trials. Red dots and solid lines represent saccades on noncanceled trials. Rows separate data by target; columns separate data by subject.

Fig. 4.

No saccadic spike potentials (SPs) are evident in canceled trials aligned on a virtual saccade event. Black traces show ERPs and colored traces show ERVs (see text). The thin solid traces show saccade-aligned ERPs and ERVs on no-stop trials. The most prominent components in the ERPs are the sharp negative SPs, which occur just before or concomitant with the saccade onset and the several positive and negative deflections that follow. The first several components that follow the saccade onset probably include a strong contribution from the corneoretinal potential. The dashed traces show ERPs and ERVs on errant noncanceled trials. Note the extreme similarity of the ERVs for no-stop and noncanceled trials. Also note the similarity between no-stop and noncanceled ERPs. This similarity is especially apparent in the time before the saccade onset when the SP is visible. The thick solid traces show ERPs and ERVs on canceled trials aligned to a virtual saccade event. No elevated velocity can be detected in the ERVs, and no SP can be detected around time 0 in the ERP. Data were collapsed across 15 sessions and recorded from a location approximating Fz for monkey F; data were collapsed across 7 sessions and recorded from a location approximating Fpz for monkey Y. ERP data were baselined to the period from 150 to 50 ms before the saccade onset. The numbers of trials (n) in each ERP were as follows: monkey F, no-stop n = 13,764, canceled n = 6,256, and noncanceled n = 6,552; and monkey Y, no-stop n = 4,782, canceled n = 1,489, and noncanceled n = 1,120.

Fig. 5.

Bandpass filters were optimized to find frequencies that allowed for the highest discrimination between the SP and non-SP components. A: 1-s example of raw EEG centered on the saccade onset. Note that in this and following panels, negative is plotted down so that later power traces appear facing upward. B: the same EEG signal processed with a 35-Hz bandpass filter. After being filtered, the analytic power was estimated (see methods), and this estimate is shown by the thick blue line. C: power at 35 Hz for every no-stop trial in the example session. Each horizontal line of color shows a single trial centered on the saccade onset. Warmer colors indicate more power. Note the faint band adjacent to the saccade onset indicating that the 35-Hz bandpass filter was somewhat successful in isolating SP-related activation. D: this result is further demonstrated by collapsing across all trials and creating an ERP from the power traces at 35 Hz. A “signal” and “noise” time period was chosen based on SP peak time measured from unfiltered session ERPs. The time period highlighted in white was the signal time period, and the time period in gray was the noise time period for monkey F. Average power in both time periods was recorded and used to calculate signal-to-noise ratios (S:N). E: the signal-to-noise ratio for each bandpass frequency was calculated for each session. These traces show the average signal-to-noise ratio separately for monkey F (blue) and monkey Y (green) ± SE. The highest signal-to-noise ratio was found at a bandpass frequency of 95 Hz for monkey F (F) and 35 Hz for monkey Y (G).

Fig. 6.

Filtering EEG makes it possible to observe the SP independent of surrounding EEG, but no SP was observed on canceled trials. Traces at the top show ERVs to display saccade timing (conventions as in Fig. 4). Heat maps show individual trials (conventions as in Fig. 5). Black lines show ERPs collapsed across trials. Thin lines show no-stop trial ERPs, and thick lines show canceled trial ERPs. The left column displays raw voltage. At the top, data are presented from no-stop trials aligned to the saccade onset. The ERV appears as a narrow component beginning at the saccade onset. The heat maps display negative bands of activation at the saccade onset corresponding to the SP. Collapsing across the data in the ERP makes the SP readily apparent in both the raw and filtered data. At the middle, data are presented from no-stop trials aligned to the target onset. The ERV reflects this change. Saccades were smeared around 200 ms centered roughly at 210 ms after the target onset. Because of this smearing, it was no longer possible to discern negative activation associated with the SP in the raw heat map. This activation should be apparent centered around 200 ms after the target onset. SP activation was also smeared in the raw ERP, rendering it invisible. However, in the filtered data, SP activation was clear around 200 ms in both the heat map and ERP. At the bottom, data are presented from canceled trials aligned to the target onset. The ERV never approached 30°/s (criteria for saccade initiation). No SPs were apparent in the raw heat map data or in the raw ERP. However, it is impossible to tell if no SPs exist, because they were also unobservable in the raw no-stop data plotted above due to overlapping components and smear. The filtered data at right allowed for an examination of SP activation. No SP activation was observed in the time around the saccade initiation. If anything, a small depression in high-frequency SP activation was all that could be observed.

Fig. 7.

No-stop trial EEGs display significantly increased SP activation during periods when saccades are produced, but canceled trial EEGs show no increase in SP activation. After trials had been latency matched and EEG data filtered (see Fig. 6), the average power during a discreet time window was measured on a trial-by-trial basis. For the time window, we chose the period between the 25th and 75th RT percentiles. Since no-stop trials were latency matched to canceled trials, this is the period of time during which SP activation was most likely to occur in both trial types. Power averages were collected from this time window at each SSD. Each SSD from each recorded session yielded a single observation for each trial type. The histograms show the results of this analysis. The observations are gathered in 0.1-μV bins for display purposes. Grand average power is reported for each trial type above the appropriate histogram. Note that the sign of these averages is negative for canceled trials. Both distributions deviated significantly from zero (Students t-test, P < 0.001, degrees of freedom = 167).