Encoding of movement direction in different frequency ranges of motor cortical local field potentials - PubMed (original) (raw)
Encoding of movement direction in different frequency ranges of motor cortical local field potentials
Jörn Rickert et al. J Neurosci. 2005.
Abstract
Recent studies showed that the low-frequency component of local field potentials (LFPs) in monkey motor cortex carries information about parameters of voluntary arm movements. Here, we studied how different signal components of the LFP in the time and frequency domains are modulated during center-out arm movements. Analysis of LFPs in the time domain showed that the amplitude of a slow complex waveform beginning shortly before the onset of arm movement is modulated with the direction of the movement. Examining LFPs in the frequency domain, we found that direction-dependent modulations occur in three frequency ranges, which typically increased their amplitudes before and during movement execution: < or =4, 6-13, and 63-200 Hz. Cosine-like tuning was prominent in all signal components analyzed. In contrast, activity in a frequency band approximately 30 Hz was not modulated with the direction of movement and typically decreased its amplitude during the task. This suggests that high-frequency oscillations have to be divided into at least two functionally different regimes: one approximately 30 Hz and one >60 Hz. Furthermore, using multiple LFPs, we could show that LFP amplitude spectra can be used to decode movement direction, with the best performance achieved by the combination of different frequency ranges. These results suggest that using the different frequency components in the LFP is useful in improving inference of movement parameters from local field potentials.
Figures
Figure 1.
Tuning of the movement-evoked potential. Time 0 ms indicates movement onset. a, Grand average mEP (averaged across all recorded LFPs). Trials were aligned either to movement onset (black curve) or to cue onset (gray curve). P1, P2, N1, and N2 indicate the points in time of the positive and negative peaks of the average LFP. b, Directional tuning of an mEP obtained from a single electrode: trial-averaged activity shown separately for each movement direction. c, Time-resolved strength of the directional modulation (signal, black curve, left vertical axis) and variance (Var.) of the trial-by-trial fluctuations (noise, gray curve, right vertical axis) for the mEPs shown in b. d, Time-resolved signal-to-noise ratio of the mEP tuning shown in b. The dotted line indicates threshold for significant tuning (p < 0.05; see Materials and Methods). The black bar below the plot shows the average time of movement end and its SD for this recording session.
Figure 2.
Cosine tuning of mEPs in the time domain. Correlations with cosine tuning curves are depicted separately for each peak (P1, N1, P2, and N2 from left to right). Data were smoothed with a Gaussian kernel of standard width of 50 ms (analysis for P1, N1, and P2) or 125 ms (analysis for N2). a, Dependence on movement direction of mean activity (black dots) and SEM (small black bars) of the sample mEPs shown in Figure 1_b_. For the peaks with significant tuning (p < 0.05; see Materials and Methods), a cosine curve was fitted to the data (black curves; see Materials and Methods for details). The time indicated above each panel is thetimerelativetomovementonset. Thenumberbeloweachcurveisthesquaredcorrelationcoefficient_r_2cosine betweendataand the fitted cosine function. b, Correlation between mEP tuning curves and fitted cosine function for all mEPs with significant tuning (p < 0.05; see Materials and Methods). The percentage of these mEPs from the total number of mEPs recorded is given in parentheses. The top panels show the distribution of values for _r_2 at P1, N1, P2, and N2, respectively. Gray histograms (bottom) depict the distribution of _r_2 values obtained for random tuning curves (see Materials and Methods).
Figure 3.
Simple model to decode LFP activity in the time domain. a, Correlation between mEP tuning curves across time. Average correlation coefficient (color coded) between two tuning curves from the same LFP recording but at different time points, given by the x and y coordinates. The bottom left half of the matrix shows the mean across all 419 LFPs; the top right half represents the average across the 56 LFPs with strongest tuning (SNR > 0.3). b, mEP of the sample LFP (Fig. 1_b_) averaged across all directions (black curve) and the LFP of a single trial (blue curve) during a movement to the left (180°) after low-pass filtering with a third-order Butterworth filter (cutoff frequency, 13 Hz). The mEP fitted the single trial activity best if multiplied by a scaling factor of 2.8 (see text for Materials and Methods as well as Results explanation). c, Distributions of amplitudes (scaling factors) obtained for all single trials belonging to a movement to the right (0°, green histogram) and to the left (180°, blue histogram).
Figure 4.
Characteristics of the LFP amplitude spectrum. Plots show averages across all electrodes and trials. a, Time-resolved amplitude spectrum (arbitrary units). The 50 Hz noise was removed by applying a notch filter centered at 50 Hz. b, Time-resolved amplitude spectrum as in a, each frequency bin normalized by its baseline amplitude (see Materials and Methods). c, Changes in amplitude exhibited by four different frequency bands (≤4, 6–13, 16–42, and 63–200 Hz) during the task.
Figure 5.
LFP tuning in the frequency domain. a, Time-resolved and normalized amplitude spectrum obtained from one sample electrode (same as in Fig. 1_b–d_), separately for each movement direction. b, Left, Normalized tuning curves (including SEMs) of the LFP amplitude spectrum shown in a for three different frequency bands (≤4, 6–13, and 63–200 Hz). Tuning curves were normalized by subtracting the mean and dividing by the SD across trials averaged across eight directions. Each tuning curve was computed at the time point in which the signal-to-noise ratio of the respective frequency band was highest (compare c). Right, Cosine functions fitted to the curves on the left. Numbers show the squared correlation coefficients between data and the fitted cosine function. c, Signal-to-noise ratios of the LFP amplitude spectrum shown in a, separately for the different frequency bands. Time is relative to movement onset. d, Distributions of SNRs across all LFPs for the ≤4, 6–13, and 63–200 Hz bands. For each LFP and frequency band, the best SNR between 200 ms before movement onset and 750 ms after movement onset was chosen. The triangle denotes the SNR values of the sample LFP.
Figure 6.
Tuning properties of LFPs in the frequency domain. a, Average tuning strength of different LFP frequency bands. Each curve depicts the time-resolved (movement onset at t = 0 ms) signal-to-noise ratio of a certain frequency band (see inset), averaged across all recorded LFPs, separately for contralateral (left) and ipsilateral (right) movements. b, Correlation between tuning curves derived from LFP amplitude spectra and best cosine fit. Only LFPs with significant tuning (p < 0.05; see Materials and Methods) in the corresponding frequency band at the selected time point were considered; their percentage is given in parentheses. Black histograms show the distribution of _r_2 values across these LFPs at P1, N1, P2, and N2 (columns, times following P1, N1, P2, and N2 denote the time relative to movement onset) and for three different frequency bands (rows). Gray histograms (bottom) show the probability distribution of _r_2 values obtained for random tuning curves (see Materials and Methods).
Figure 7.
Signal and noise correlation between two different frequency bands. Time 0 ms indicates movement onset. a, Noise correlations. Correlation between trial-by-trial fluctuations of two different frequency bands (indicated on top) for all combinations of time delay between the two bands is shown. x and y coordinates indicate the time point of measurement for the second and the first frequency bands, respectively. Data were averaged across all recorded LFPs. b, Signal correlation. Correlation between the tuning curves of two different frequency bands (indicated at the top) for all combinations of time delay between the two bands is shown. x and y coordinates indicate the time point of measurement of tuning curves for the second and the first frequency bands, respectively. Data were averaged across all recorded LFPs, with significant tuning (p < 0.01) occurring in both bands during the course of the task.
Figure 8.
Decoding power of different frequency bands. a, The box plots show the distribution of decodingm power of single LFPs for various frequency bands and their combinations indicated at the bottom. White bars depict the median, the box ranges from the lower to the upper quartiles, the dashed whiskers extend to the most extreme decoding power within the 1.5-fold interquartile range from the borders of the bars, and the × symbols mark outliers. b, Decoding power of simultaneous LFP recordings from eight electrodes (symbols as in a).
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