Manifestation of ocular-muscle EMG contamination in human intracranial recordings

Abstract

It is widely assumed that intracranial recordings from the brain are only minimally affected by contamination due to ocular-muscle electromyogram (oEMG). Here we show that this is not always the case. In intracranial recordings from five surgical epilepsy patients we observed that eye movements caused a transient biphasic potential at the onset of a saccade, resembling the saccadic spike potential commonly seen in scalp EEG, accompanied by an increase in broadband power between 20 and 200 Hz. Using concurrently recorded eye movements and high-density intracranial EEG (iEEG) we developed a detailed overview of the spatial distribution and temporal characteristics of the saccade-related oculomotor signal within recordings from ventral, medial and lateral temporal cortex. The occurrence of the saccadic spike was not explained solely by reference contact location, and was observed near the temporal pole for small (<2 deg) amplitude saccades and over a broad area for larger saccades. We further examined the influence of saccade-related oEMG contamination on measurements of spectral power and interchannel coherence. Contamination manifested in both spectral power and coherence measurements, in particular, over the anterior half of the ventral and medial temporal lobe. Next, we compared methods for removing the contaminating signal and found that nearest-neighbor bipolar re-referencing and ICA filtering were effective for suppressing oEMG at locations far from the orbits, but tended to leave some residual contamination at the temporal pole. Finally, we show that genuine cortical broadband gamma responses observed in averaged data from ventral temporal cortex can bear a striking similarity in time course and band-width to oEMG contamination recorded at more anterior locations. We conclude that eye movement-related contamination should be ruled out when reporting high gamma responses in human intracranial recordings, especially those obtained near anterior and medial temporal lobe.

Figure 1

Sequence of events in a trial. A fixation cross is presented for 1 to 2 seconds, followed by a search array of pseudorandomly positioned faces for 4 seconds, followed by a probe face for 1 second. Subjects indicate with a button press whether the probe face matched any face in the preceding array with respect to orientation, identity and facial expression.

Figure 2

The intracranial Saccadic Spike Potential. A: Saccadic spikes observed in unaveraged 20–200 Hz filtered field potential (black line) from a contact near temporal pole. The top two plots show horizontal and vertical gaze position. Yellow lines indicate extracted saccade onset times. Note that the second saccade onset most likely represents a false positive. B: Morphology of the iSSP averaged with respect to saccade onset in an intracranial channel (blue line) and as observed in extracranial EOG contact (black line). In both cases data are bandpass filtered from 20 to 200 Hz. Average rectified unfiltered EOG (red) shows the time course of the iSSP in relation to onset of eye movement. C: iSSP morphology in all five subjects observed in the channel with maximal peak-to-trough iSSP amplitude. In all subjects the maximal iSSP amplitude appeared in channels near the temporal pole

Figure 3

Manifestation of iSSP in subdural ECoG recordings. Peak-to-trough iSSP amplitude for all subjects and ECoG recording locations is shown at center. A. Peak-to-trough amplitude of iSSP for all channels which reached statistical significance at FDR q-value = 0.01. Channels which did not reach the significance criterion are unfilled. Six example waveforms are displayed for the indicated contacts. Note that the vertical scale for the waveforms from posterior contacts differs from anterior contacts in order to aid visibility. B. Peak-to-trough amplitude interpolated over all contacts and subjects.

Figure 4

Manifestation of iSSP in depth recordings from anterior temporal lobe and Heschl’s gyrus. In four contact depth electrodes targeted to left (all subjects) and right (subjects 3, 4 and 5) amygdala (circles), large amplitude iSSPs are observed at medial contacts. Smaller iSSPs appear at contacts in Heschl’s gyrus (triangles). Left and right columns show mean iSSP for each contact arranged in left-to-right order under common subgaleal reference (black) and after bipolar rereferencing between neighboring channels (gray). Contact location is shown in the central column, where color indicates subject identity. As in the subdural ECoG electrodes, a large medio-lateral gradient is apparent in iSSP amplitude. Eye and extraocular muscle (medial, lateral, superior and inferior rectus) position are shown schematically with green ellipses and red lines, respectively. The most medial right-sided contact for subject 5 was broken and is not shown.

Figure 5

iSSP peak-to-trough amplitude dependence on saccade amplitude and direction. Peak-to-trough amplitudes in unaveraged data, normalized within each subject to the mean iSSP amplitude for all saccades over 10 deg. Data are taken from the channel with the largest iSSP, which was a contact near temporal pole in each subject, normalized and pooled across subjects. Mean iSSP amplitude as a function of saccade amplitude and 2 S.E.M are shown for ipsiversive saccades (red), contraversive saccades (blue) and all saccades (purple) in data pooled across subjects. Curves are fitted by an eighth order polynomial, with the order chosen to minimize AIC. iSSP amplitude increases approximately linearly for small amplitude saccades under 5 deg, approaching a plateau beyond 6 degrees. In all subjects ipsiversive saccades generated a larger iSSP than contraversive at the selected temporal pole contact. Mean iSSP amplitude over all saccades in each case is shown by the dashed lines of corresponding color. The histogram shows the relative frequency of saccades as a function of eccentricity.

Figure 6

Dependence of the distribution and peak-to-trough amplitude of saccadic spikes on saccade amplitude. The color scale shows mean iSSP peak-to-trough amplitude for saccades which fall within the given amplitude range. Only channels which reached an FDR corrected significance threshold q ≤ .01 are filled.

Figure 7

Dependence of peak-to-trough iSSP amplitude on saccade amplitude across channels. Mean peak-to-trough amplitude is shown for saccades which fall within the given amplitude range. Responses are colored red if they are significantly different from 0 at FDR corrected significance threshold q ≤ .01. Values at the top of each panel show the number of channels, out of 128, meeting the significance criterion within each interval.

Figure 8

Independent Component Analysis to remove the iSSP related signal. A. Distribution of mixing weights for the component with the largest iSSP related gamma band spectral perturbation of band power. B. iSSP waveform in the independent component with the largest perisaccadic perturbation (shown for each of the five patients). For both A and B the units of components and weights returned by ICA are arbitrary and have therefore been normalized within each subject to the maximum weight across all channels in the former case and to the peak-to-trough difference in the latter. C. Decrease in perisaccadic 20–200 Hz log spectral perturbation for the channel with the largest iSSP after removing the k^th sorted IC component (sorted by perisaccadic perturbation), normalized for each subject (different colors) to log change after removing the first component.

Figure 9

Effect of ICA filtering (rows) and bipolar rereferencing (columns) on iSSP peak-to-trough amplitude. Data in the left column are in the original common reference space. In the right column, data have been rereferenced to neighboring contacts within at most 1 cm, indicated by elongated bars. The top row shows amplitude without ICA filtering, the second row after removing the first sorted independent component, and the third row after removing the first and second sorted independent component. Contacts for which the response does not reach significance threshold of FDR q = 0.01 are unfilled.

Figure 10

Contribution of the filtered components to trial onset related 70–100Hz band-response. A. Mean log band power increase (dB) in the 0 –500 ms epoch after stimulus onset, normalized to the −400 to −100 ms epoch. Channels for which significance didn’t reach a threshold of FDR q = 0.01 are unfilled. B. Response after ICA filtering. C. Summary of significance tests in A and B: contacts are colored green if the response remains significant (FDR q = 0.01) before and after filtering, red if the response is significant only before filtering but not after, and blue if the response is significant after filtering but not before. D. Contribution of filtered independent components to trial onset response log power, measured as the decibel log-ratio of power in the 0–500 ms epoch between ICA filtered and unfiltering data. E. Average log band power for the entire duration of the trial in selected channels, before ICA filtering (red) and after filtering (blue). Selected channels are from temporal pole (TP), mesial ventral temporal cortex, middle section (MVTM), lateral ventral temporal cortex, middle section (MVTL) and posterior ventral temporal cortex (PVT). Time points when the difference between the unfiltered and filtered response is significant (FDR q = 0.01) are shown by thick black line segments along the x-axis.

Figure 11

Effect of ICA filtering on trial onset responses in depth recordings. The change in 70–100Hz power following task onset, normalized to respective filtered and unfiltered baselines, is shown for the common reference (A) and after nearest-neighbor rereferencing (B). The contributions of filtered components to signal power (log ratio of power without normalizing to baselines, as in Fig. 10D) following trial onset are shown in C and D.

Figure 12

Log power wavelet spectrograms showing average trial onset related spectral perturbation at temporal pole (contact TP, labeled in figure 10), mesial ventral temporal cortex (contact MVTM), middle section, and posterior ventral temporal cortex (PVT). Thick black lines indicate significance regions for FDR q = 0.001 and thin black lines for q = 0.05. Left column shows response before ICA filtering, middle column after filtering, and right column shows the difference of the two. The top left panel shows the histogram of saccade onsets within 50 ms bins.

Figure 13

Log power wavelet spectrograms showing average saccade related spectral perturbation (averaged with respect to saccade onsets detected by eye tracker) for the same contacts as in Figure 10 and 12. Power is normalized to the −500 – −200 ms epoch preceding saccade onset. Thick black lines indicate significance regions for FDR q = 0.001 and thin black lines for q = 0.05. Left column shows response before ICA filtering, middle column after filtering, and right column shows the difference of the two. The top left panel shows the histogram of saccade onsets within 5 ms bins. The post-saccadic refractory period following the previous saccade, falling within the preceding fixation, is shown (green line), as well as the perisaccadic window (red line).

Figure 14

An example of similarity in the time course of oEMG related responses and cortical response. Trial onset related increase in 70–100 Hz band power in the temporal pole (contact TP, green) are closely associated with eye movements, while the response observed in posterior ventral temporal contacts is not (PVT, magenta). A: Both responses have a similar time-course including a peak at 240 ms, as well as magnitude with respect to baseline. Contacts adjacent to PVT (gray and black) also show a similar pattern, although with different amplitudes and latencies in the initial peak. B: Sorting trials by the delay to the first saccade reveals that the response is strongly time-locked to saccade onset (black line) in TP (top) but not in PVT (bottom). The data were smoothed over trials with a five point moving average applied after sorting.

Figure 15

Perisaccadic changes in interchannel coherence caused by oEMG contamination. Change in mean 70 – 100 Hz interchannel coherence between the saccade-onset window (100 ms centered at the saccade onset; red bar in Figure 13) and a preceding reference period (preceding 100ms; green bar in Figure 13) in the original data (A), after bipolar rereferencing (B), and after ICA filtering (C). Saccade onset associated change in coherence pooled across all channels and subjects. D. The histograms for mean coherence between 40 and 100 Hz in the presaccadic (green) and saccade onset (red) windows. E. The difference between the histogram of coherences over all channels and subjects broken down by frequency. A difference is visually most apparent between 40 and 100 Hz (bracket on the right side) and is confirmed by a one tailed rank sum test on the medians. The grayscale bar at left shows the result of a one-tailed rank sum test; frequencies at which median coherence in the saccade onset window significantly exceeds that of the presaccadic window at uncorrected P < .001 are tagged white and are tagged gray for P < .05.