Spectral changes in cortical surface potentials during motor movement

Abstract

In the first large study of its kind, we quantified changes in electrocorticographic signals associated with motor movement across 22 subjects with subdural electrode arrays placed for identification of seizure foci. Patients underwent a 5-7 d monitoring period with array placement, before seizure focus resection, and during this time they participated in the study. An interval-based motor-repetition task produced consistent and quantifiable spectral shifts that were mapped on a Talairach-standardized template cortex. Maps were created independently for a high-frequency band (HFB) (76-100 Hz) and a low-frequency band (LFB) (8-32 Hz) for several different movement modalities in each subject. The power in relevant electrodes consistently decreased in the LFB with movement, whereas the power in the HFB consistently increased. In addition, the HFB changes were more focal than the LFB changes. Sites of power changes corresponded to stereotactic locations in sensorimotor cortex and to the results of individual clinical electrical cortical mapping. Sensorimotor representation was found to be somatotopic, localized in stereotactic space to rolandic cortex, and typically followed the classic homunculus with limited extrarolandic representation.

Figure 1.

Demonstration of the analysis technique for a hand movement task in patient 5. The shaded areas in the spectral plot illustrate the bands used for analysis. The green shaded region is from 8 to 32 Hz (LFB), and the orange shaded region is from 76 to 100 Hz (HFB). The top cortical map shows the activation distribution for the HFB (here, reflecting an increase in spectral power with movement). The bottom map, for the LFB, shows a decrease in spectral power with movement over a broader set of electrodes. The color bar indicates the scale used for all spectral maps: blues reflect spectral decrease, and red–yellow reflects spectral increase. Gray indicates no change. All cortical maps are scaled to the maximum increase or decrease; thus, there is no relevant absolute scale. Electrode locations are shown in white.

Figure 2.

The power spectra for the motor task (red) and rest intervals (blue) illustrate the rationale and tentative hypothesis behind the choice of spectral bands (HFB and LFB) for analysis. A–D, The first three plots (A–C) are elements of artificial schema, and the fourth (D) is actual data (the same as in Fig. 2). A, Modeling the ERD. In the rest condition, it is proposed that native timescales of 200 and 50 ms, generating spectral peaks based at 5 and 20 Hz, arise from cortical regulation by thalamus and/or other structures. With motor activation, one or more of these timescales decohere (“desynchronize”). Note that the rest period here does not necessarily reflect a baseline state, but the rest interval between actions, and may therefore be more coherent (“synchronized”) than a true baseline state. The schematic assumes 99% decoherence of the 20 Hz spectral peak with respect to the resting state. The green band reflects the analysis band (LFB) used to capture this effect. B, Modeling the broad spectral increase. In this model, a power law spectral shift from, for example, 1/f^2.3 in the rest state to 1/f² in the motor state, is diagrammed. This broad increase could also be a result of white noise addition to the data (a uniform shift upward). The orange band (HFB) is chosen to capture this shift because it is away from masking by discrete, native, timescales at lower frequencies (as in A) and noise contamination at 60 Hz. C, Superposition of the spectra in A and B, with the addition of 60 Hz noise (the same amount to each state). The orange and green bands are as before. D, Actual shift seen. This spectrum is the same as in Figure 2. Note the similarity to the modeled spectrum (C).

Figure 3.

Grid placement and representation on a brain template. A, B, The brain is exposed (A) and electrodes are placed in the subdural space (B) to identify seizure onset and map cortex for clinical purposes before resection of epileptic focus. C, D, The electrodes are localized with a lateral skull x ray (Miller et al., 2007) (C), and positions transformed to a standardized template (D). White dots represent the center of the electrode location in the standardized Talairach coordinate system (Talairach and Tournoux, 1988).

Figure 4.

Spectra superimposed on the brain over each electrode for patient JC during a hand movement task (red curves) and resting interval (blue curves). The frequency range (see top left inset) is 8–100 Hz. Note that 60 Hz noise varies across electrodes (the two chosen frequency bands are away from this artifact). The bottom cortical insets reflect the generated cortical activation maps, with the HFB map on the left cortex and the LFB map on the right. Note that, as expected by the bottom insets, the most dramatic effects in the individual spectra are seen in the top, middle portions of the grid.

Figure 5.

Cortical activation maps for hand and tongue movements. Electrode locations are shown in white. The top cortex of each pair is the HFB activation, and the bottom is the LFB activation. Outer brains, Individual patients are reflected by brain pairs around the outside of the figure, with the number next to the brain indicating the patient number, as detailed in Table 1. Central brains, The average activations for hand and tongue movement for left and right cortices (right and left hand movement, depending on the patient's electrode locations).

Figure 6.

For details, see Figure 5.

Figure 7.

Average representation with contralateral electrode locations mirrored to one side (left brain). Each is scaled for the maximum increase or decrease. The somatotopic distribution of the activations is evident comparing the hand (left) and tongue (right). Additionally, there is qualitatively less spatial overlap between the HFB representations (top) than the LFB (bottom). The qualitative properties of each type of activation are detailed in Table 2. Please see the supplemental discussion for more depth about types of interpolation across individuals and why this particular technique was chosen.

Figure 8.

Five different movement modalities within the same patient for three different patients, with each relevant modality labeled. The top brains are high-frequency band representation, and the bottom are low-frequency representation. White dots indicate electrode positions, and the green triangles reflect the pairwise stimulation sites, which elicited movement of the concerned modality. A–C, Data for subjects 9 (A), 3 (B), and 16 (C) are shown. The medial representations in C reflect activation as reflected by a 2 × 8 interhemispheric strip, and the activations seen are likely supplementary motor areas rather than sensorimotor cortex.

Figure 9.

Four magnified brain maps to show stimulation resulting in motor movement along with the activation for the same modality. Stimulation is done pairwise; thus, elicited motor movement may be attributable to cortex beneath only one of the electrode pair. Positive electrode stimulation locations are shown with green triangles connected by jagged green lines. The top cortex of each pair is the high-frequency representation, and the bottom is the low-frequency representation. A, B, Hand movements with stimulation are shown for patients 16 (A) and 6 (B). C, D, Tongue movements are shown for patients 1 (C) and 3 (D). Please see the supplemental discussion (available at www.jneurosci.org as supplemental material) regarding the stimulation process.