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Cited by 134Neural dynamics and brain functionMotor Control and AdaptationDeep Brain Stimulation and Movement Disorders

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A Common Structure Underlies Low-Frequency Cortical Dynamics in Movement, Sleep, and Sedation

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Hall, Thomas M., de Carvalho, Felipe, Jackson, Andrew·2014·Neuron
DOI 10.1016/j.neuron.2014.07.022PMC PMC4157580
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Abstract

Upper-limb movements are often composed of regular submovements, and neural correlates of submovement frequencies between 1 and 4 Hz have been found in the motor cortex. The temporal profile of movements is usually assumed to be determined by extrinsic factors such as limb biomechanics and feedback delays, but another possibility is that an intrinsic rhythmicity contributes to low frequencies in behavior. We used multielectrode recordings in monkeys performing an isometric movement task to reveal cyclic activity in primary motor cortex locked to submovements, and a distinct oscillation in premotor cortex. During ketamine sedation and natural sleep, cortical activity traversed similar cycles and became synchronized across areas. Because the same cortical dynamics are coupled to submovements and also observed in the absence of behavior, we conclude that the motor networks controlling the upper limb exhibit an intrinsic periodicity at submovement frequencies that is reflected in the speed profile of movements.

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Figure 1 Low-Frequency Cortical Dynamics during Isometric Task Performance (A) Schematic of isometric wrist-torque task. (B) Top: position of cursor (solid lines) and target (dashed lines) during a typical trial. Middle: cursor speed (time derivative of radial position from the origin). Bottom: raw (black) and rectified, smoothed (red; not to scale) EMG from a wrist extensor muscle, extensor carpi ulnaris (ECU). Five submovements occurred during this trial, indicated by arrowheads. (C) Top: unfiltered, surface-referenced LFP from a representative electrode in M1 during task performance. Middle: low-pass-filtered, mean-subtracted LFP from all electrodes in the M1 array, ordered and color coded according to phase relative to submovements. The bottom trace (blue) corresponds to the unfiltered signal shown at the top (black). Bottom: spike rasters for seven M1 neurons. (D) Top: first two principal components (LFP-PCs) calculated from low-pass-filtered, mean-subtracted M1 LFP. Bottom: second LFP-PC and speed profile overlaid. Data are from monkey D. See also Movie S1.
Figure 1 Low-Frequency Cortical Dynamics during Isometric Task Performance (A) Schematic of isometric wrist-torque task. (B) Top: position of cursor (solid lines) and target (dashed lines) during a typical trial. Middle: cursor speed (time derivative of radial position from the origin). Bottom: raw (black) and rectified, smoothed (red; not to scale) EMG from a wrist extensor muscle, extensor carpi ulnaris (ECU). Five submovements occurred during this trial, indicated by arrowheads. (C) Top: unfiltered, surface-referenced LFP from a representative electrode in M1 during task performance. Middle: low-pass-filtered, mean-subtracted LFP from all electrodes in the M1 array, ordered and color coded according to phase relative to submovements. The bottom trace (blue) corresponds to the unfiltered signal shown at the top (black). Bottom: spike rasters for seven M1 neurons. (D) Top: first two principal components (LFP-PCs) calculated from low-pass-filtered, mean-subtracted M1 LFP. Bottom: second LFP-PC and speed profile overlaid. Data are from monkey D. See also Movie S1.CC BY · PubMed Central
Figure 2 Relationship between LFP-PCs and Movement Kinematics (A) Intersubmovement interval histograms for representative sessions in all three animals. (B) Autocorrelation histogram of intervals between all pairs of submovements in the same trial (between go cue and end of successful hold). Histograms are normalized by the interval distribution expected for a uniform (Poisson) distribution with the same rate. The peak at around 300 ms reveals the underlying rhythmicity of submovements. (C) Coherence spectra between radial cursor position and rectified EMG from four wrist muscles: extensor carpi ulnaris (ECU), extensor carpi radialis (ECR), flexor carpi ulnaris (FCU), and flexor carpi radialis (FCR). Data are from monkey D comprising 320 trials with 2,063 submovements. (D) Coherence spectra between LFP-PCs and radial cursor speed across the same session. (E) LFP-PC trajectory for 2 s of the representative trial shown in Figure 1. Circles indicate times of peak cursor speed. (F) LFP-PC trajectories aligned to peak speed of submovements and averaged across nine equal-sized groups sorted by peak cursor speed. Trajectories are plotted for 200 ms on either side of time of peak speed (indicated by circles) and color coded from black to red to yellow according to cursor speed. (G) Rotational frequency of average trajectories for different submovement speeds, calculated at the time of peak cursor speed. (H) Areal velocity (area swept out per unit time) of average trajectories for different submovement speeds, calculated at the time of peak cursor speed. (I–K) Equivalent analysis of a representative session with monkey R comprising 150 trials with 823 submovements. (L) Average 2D LFP-PC trajectories for submovements, binned and color coded according to the direction of cursor movement. Arrows in the inset indicate the central direction of movement for each bin. (M) Average LFP-PC trajectories in the plane of PC2 and PC3. The trajectories revolve around slightly different angular velocity vectors, indicated by arrows. (N) Angular coefficient of determination for submovement direction, decoded from the orientation of LFP-PC angular velocity. Leave-one-out cross-validation was performed over every submovement in each data set. The plot shows the average CoD for validation submovements in each speed group, based on data from 13 sessions in three monkeys. Also shown is the average 95% percentile from shuffled data. See also Movies S2 and S3.
Figure 2 Relationship between LFP-PCs and Movement Kinematics (A) Intersubmovement interval histograms for representative sessions in all three animals. (B) Autocorrelation histogram of intervals between all pairs of submovements in the same trial (between go cue and end of successful hold). Histograms are normalized by the interval distribution expected for a uniform (Poisson) distribution with the same rate. The peak at around 300 ms reveals the underlying rhythmicity of submovements. (C) Coherence spectra between radial cursor position and rectified EMG from four wrist muscles: extensor carpi ulnaris (ECU), extensor carpi radialis (ECR), flexor carpi ulnaris (FCU), and flexor carpi radialis (FCR). Data are from monkey D comprising 320 trials with 2,063 submovements. (D) Coherence spectra between LFP-PCs and radial cursor speed across the same session. (E) LFP-PC trajectory for 2 s of the representative trial shown in Figure 1. Circles indicate times of peak cursor speed. (F) LFP-PC trajectories aligned to peak speed of submovements and averaged across nine equal-sized groups sorted by peak cursor speed. Trajectories are plotted for 200 ms on either side of time of peak speed (indicated by circles) and color coded from black to red to yellow according to cursor speed. (G) Rotational frequency of average trajectories for different submovement speeds, calculated at the time of peak cursor speed. (H) Areal velocity (area swept out per unit time) of average trajectories for different submovement speeds, calculated at the time of peak cursor speed. (I–K) Equivalent analysis of a representative session with monkey R comprising 150 trials with 823 submovements. (L) Average 2D LFP-PC trajectories for submovements, binned and color coded according to the direction of cursor movement. Arrows in the inset indicate the central direction of movement for each bin. (M) Average LFP-PC trajectories in the plane of PC2 and PC3. The trajectories revolve around slightly different angular velocity vectors, indicated by arrows. (N) Angular coefficient of determination for submovement direction, decoded from the orientation of LFP-PC angular velocity. Leave-one-out cross-validation was performed over every submovement in each data set. The plot shows the average CoD for validation submovements in each speed group, based on data from 13 sessions in three monkeys. Also shown is the average 95% percentile from shuffled data. See also Movies S2 and S3.CC BY · PubMed Central
Figure 3 Low-Frequency Cortical Dynamics during Ketamine Sedation, Natural Sleep, and Free Reaching (A) EMG, unfiltered LFP, processed LFP, and spike rasters during ketamine sedation following the session in Figure 1. Arrowheads indicate K complexes, sometimes associated with spindles (∗). LFP traces are ordered and color coded as in Figure 1. (B) Equivalent recordings during natural sleep at the end of the session in Figure 1. (C) Equivalent recordings during retrieval of food from small wells in a Klüver board. In addition to the wrist muscles named in Figure 2, EMG was recorded from flexor digitorum profundus (FDP), flexor digitorum superficialis (FDS), and first dorsal interosseous (1DI), which act on the fingers. (D) Coherence spectra between M1 LFP-PCs and wrist and finger muscles during free reaching exhibit low-frequency coherence peaks.
Figure 3 Low-Frequency Cortical Dynamics during Ketamine Sedation, Natural Sleep, and Free Reaching (A) EMG, unfiltered LFP, processed LFP, and spike rasters during ketamine sedation following the session in Figure 1. Arrowheads indicate K complexes, sometimes associated with spindles (∗). LFP traces are ordered and color coded as in Figure 1. (B) Equivalent recordings during natural sleep at the end of the session in Figure 1. (C) Equivalent recordings during retrieval of food from small wells in a Klüver board. In addition to the wrist muscles named in Figure 2, EMG was recorded from flexor digitorum profundus (FDP), flexor digitorum superficialis (FDS), and first dorsal interosseous (1DI), which act on the fingers. (D) Coherence spectra between M1 LFP-PCs and wrist and finger muscles during free reaching exhibit low-frequency coherence peaks.CC BY · PubMed Central
Figure 4 Submovement- and K Complex-Related Activity Share a Common Low-Frequency Phase Structure (A) Left: average cursor speed aligned to a peak speed of 2,063 submovements. Right: average surface-referenced unfiltered LFP aligned to the peak of 197 K complexes. Data are from monkey D, same sessions as in Figures 1 and 3. (B) Average normalized firing rate of seven neurons in M1 (blue) and six neurons in PMv (red) relative to submovement (left) and K complex (right). (C) Average low-pass-filtered, mean-subtracted LFP from ten M1 electrodes relative to submovement (left) and K complex (right). Traces in both plots are color coded according to phase relative to submovements. (D) Average submovement-triggered (left) and K complex-triggered (right) LFP-PC trajectories, plotted over 200 ms on either side of the trigger event (indicated by circles). All data are projected onto the PC axes determined from LFPs recorded during isometric task performance. (E) LFP phase relative to submovement (SM phase) plotted against LFP phase relative to K complex (KC phase) for each M1 electrode (unwrapped over two full cycles). Dashed lines indicate equality. Points are color coded according to LFP phase relative to submovements. (F) SM phase plotted against KC phase for all LFP recordings over 13 sessions in three monkeys. Data are presented in Table S2. See also Figure S1.
Figure 4 Submovement- and K Complex-Related Activity Share a Common Low-Frequency Phase Structure (A) Left: average cursor speed aligned to a peak speed of 2,063 submovements. Right: average surface-referenced unfiltered LFP aligned to the peak of 197 K complexes. Data are from monkey D, same sessions as in Figures 1 and 3. (B) Average normalized firing rate of seven neurons in M1 (blue) and six neurons in PMv (red) relative to submovement (left) and K complex (right). (C) Average low-pass-filtered, mean-subtracted LFP from ten M1 electrodes relative to submovement (left) and K complex (right). Traces in both plots are color coded according to phase relative to submovements. (D) Average submovement-triggered (left) and K complex-triggered (right) LFP-PC trajectories, plotted over 200 ms on either side of the trigger event (indicated by circles). All data are projected onto the PC axes determined from LFPs recorded during isometric task performance. (E) LFP phase relative to submovement (SM phase) plotted against LFP phase relative to K complex (KC phase) for each M1 electrode (unwrapped over two full cycles). Dashed lines indicate equality. Points are color coded according to LFP phase relative to submovements. (F) SM phase plotted against KC phase for all LFP recordings over 13 sessions in three monkeys. Data are presented in Table S2. See also Figure S1.CC BY · PubMed Central
Figure 5 Consistent Low-Frequency LFP Dynamics across Behavioral Conditions (A) Power spectrum of unfiltered M1 LFPs during isometric task performance, free reaching, natural sleep, and ketamine sedation. (B) Cross-correlation (normalized R values for each time lag) between unfiltered (left) and low-pass-filtered (right) LFP-PCs under four behavioral states. All data are projected onto the PC axes determined from low-frequency LFPs recorded during isometric task performance. (C) Average frequency of LFP-PC correlation (determined from the time interval between cross-correlation peak and trough) for monkeys D and S. In both animals a small but consistent reduction in frequency is observed during free reaching and ketamine sedation. (D) Coefficient of determination for a linear dynamical model fit to delta band (black) and beta band (gray). The plot compares the quality of the model fitted on isometric task data and tested on the same task data (task fit), the model fitted on task data and tested on sedation data (task-sedation generalization), and the model fitted to sedation data and tested on sedation data (sedation fit). Thirteen session pairs in three animals; data are presented in Table S3. (E) Equivalent plot showing the model fitted on isometric task data generalizes to natural sleep. Nine session pairs in two animals; data are presented in Table S4. (F) Equivalent plot showing the model fitted on isometric task data generalizes to free reaching. Ten session pairs in two animals; data are presented in Table S5. Error bars indicate SD. N.S., not significant, p > 0.05; ∗p < 0.05; ∗∗p < 0.01; ∗∗∗p < 0.001; paired t test.
Figure 5 Consistent Low-Frequency LFP Dynamics across Behavioral Conditions (A) Power spectrum of unfiltered M1 LFPs during isometric task performance, free reaching, natural sleep, and ketamine sedation. (B) Cross-correlation (normalized R values for each time lag) between unfiltered (left) and low-pass-filtered (right) LFP-PCs under four behavioral states. All data are projected onto the PC axes determined from low-frequency LFPs recorded during isometric task performance. (C) Average frequency of LFP-PC correlation (determined from the time interval between cross-correlation peak and trough) for monkeys D and S. In both animals a small but consistent reduction in frequency is observed during free reaching and ketamine sedation. (D) Coefficient of determination for a linear dynamical model fit to delta band (black) and beta band (gray). The plot compares the quality of the model fitted on isometric task data and tested on the same task data (task fit), the model fitted on task data and tested on sedation data (task-sedation generalization), and the model fitted to sedation data and tested on sedation data (sedation fit). Thirteen session pairs in three animals; data are presented in Table S3. (E) Equivalent plot showing the model fitted on isometric task data generalizes to natural sleep. Nine session pairs in two animals; data are presented in Table S4. (F) Equivalent plot showing the model fitted on isometric task data generalizes to free reaching. Ten session pairs in two animals; data are presented in Table S5. Error bars indicate SD. N.S., not significant, p > 0.05; ∗p < 0.05; ∗∗p < 0.01; ∗∗∗p < 0.001; paired t test.CC BY · PubMed Central
Figure 6 M1 and PMv Are Active during Distinct Phases of Isometric Task Performance (A) Radial cursor position for a representative trial of the isometric task. After the peripheral target is acquired (End hold), the monkey takes a food reward with the hand ipsilateral to the recording sites. Also shown is raw (black) and rectified, smoothed (red; not to scale) EMG from a wrist extensor muscle, in which the submovement structure is more clearly evident. (B) Spike rasters for eight neurons in M1 (blue) and six neurons in PMv (red). Note that M1 neurons fire with contralateral isometric wrist submovements, whereas PMv neurons are active as the monkey takes food with the ipsilateral limb. (C) Low-pass-filtered, mean-subtracted LFPs recorded from ten electrodes in M1 and eight electrodes in PMv. (D) LFP-PCs calculated from M1 and PMv recordings. (E) Radial cursor speed and M1 LFP-PC2 overlaid. Arrowheads indicate identified submovements with a peak speed exceeding 30%/s. Note that submovements are phase locked to the M1 oscillation, although in this trial they do not occur on every cycle. (F) Areal velocity in the PC plane for M1 and PMv LFPs. Increased areal velocity in M1 coincides with M1 neural activity, whereas increased areal velocity in PMv coincides with PMv neural activity. (G) Cross-correlation between LFP-PCs within the same cortical area. (H) Cross-correlation between LFP-PCs across cortical areas. Data are from monkey D. See also Figures S3 and S4.
Figure 6 M1 and PMv Are Active during Distinct Phases of Isometric Task Performance (A) Radial cursor position for a representative trial of the isometric task. After the peripheral target is acquired (End hold), the monkey takes a food reward with the hand ipsilateral to the recording sites. Also shown is raw (black) and rectified, smoothed (red; not to scale) EMG from a wrist extensor muscle, in which the submovement structure is more clearly evident. (B) Spike rasters for eight neurons in M1 (blue) and six neurons in PMv (red). Note that M1 neurons fire with contralateral isometric wrist submovements, whereas PMv neurons are active as the monkey takes food with the ipsilateral limb. (C) Low-pass-filtered, mean-subtracted LFPs recorded from ten electrodes in M1 and eight electrodes in PMv. (D) LFP-PCs calculated from M1 and PMv recordings. (E) Radial cursor speed and M1 LFP-PC2 overlaid. Arrowheads indicate identified submovements with a peak speed exceeding 30%/s. Note that submovements are phase locked to the M1 oscillation, although in this trial they do not occur on every cycle. (F) Areal velocity in the PC plane for M1 and PMv LFPs. Increased areal velocity in M1 coincides with M1 neural activity, whereas increased areal velocity in PMv coincides with PMv neural activity. (G) Cross-correlation between LFP-PCs within the same cortical area. (H) Cross-correlation between LFP-PCs across cortical areas. Data are from monkey D. See also Figures S3 and S4.CC BY · PubMed Central
Figure 7 M1 and PMv Activity during Isometric Task Performance and Ketamine Sedation (A) Radial cursor position aligned to the end of successful hold periods for peripheral targets, averaged across 40 trials from the session shown in Figure 6. (B) Average normalized (to zero mean and unity standard deviation) firing rate for eight M1 neurons and six PMv neurons, aligned to the end of the hold period. M1 activity is highest as the monkey generates torque with the contralateral wrist to reach targets. PMv activity is highest after the successful trial, corresponding to taking food reward with the ipsilateral limb. (C) Average areal velocity in the PC plane of M1 and PMv LFPs, aligned to the end of the hold period. The profile of areal velocity during task performance mirrors the dissociation seen in neural activity across areas. Note that the vertical scale for PMv areal velocity is expanded ×2 for ease of comparison. (D) Average unfiltered, surface-referenced M1 LFP aligned to the peak of 48 K complexes during ketamine sedation. (E) Average normalized firing rate for the same M1 and PMv neurons, aligned to K complexes. Neural activity in both M1 and PMv is maximal during the rising phase and peak of the K complexes. (F) Average areal velocity in the PC plane of M1 and PMv LFPs, aligned to K complexes. Shading indicates SEM across trials or K complexes.
Figure 7 M1 and PMv Activity during Isometric Task Performance and Ketamine Sedation (A) Radial cursor position aligned to the end of successful hold periods for peripheral targets, averaged across 40 trials from the session shown in Figure 6. (B) Average normalized (to zero mean and unity standard deviation) firing rate for eight M1 neurons and six PMv neurons, aligned to the end of the hold period. M1 activity is highest as the monkey generates torque with the contralateral wrist to reach targets. PMv activity is highest after the successful trial, corresponding to taking food reward with the ipsilateral limb. (C) Average areal velocity in the PC plane of M1 and PMv LFPs, aligned to the end of the hold period. The profile of areal velocity during task performance mirrors the dissociation seen in neural activity across areas. Note that the vertical scale for PMv areal velocity is expanded ×2 for ease of comparison. (D) Average unfiltered, surface-referenced M1 LFP aligned to the peak of 48 K complexes during ketamine sedation. (E) Average normalized firing rate for the same M1 and PMv neurons, aligned to K complexes. Neural activity in both M1 and PMv is maximal during the rising phase and peak of the K complexes. (F) Average areal velocity in the PC plane of M1 and PMv LFPs, aligned to K complexes. Shading indicates SEM across trials or K complexes.CC BY · PubMed Central
Figure 8 Phase Locking of Neural Activity to the Cortical Cycle during Isometric Movement, Free Reaching, Natural Sleep, and Ketamine Sedation (A) Spike-triggered average LFP-PC trajectories for eight M1 neurons (blue) and six PMv neurons (red) over 200 ms before and after spike time (indicated by circles). Top row: averages of M1 LFPs; bottom row: averages of PMv LFPs. In all cases, the data are projected onto PC axes determined from the isometric task recordings. Nevertheless, a consistent rotational structure is observed across all behavioral states. See also Movie S5. (B) Summary of the preferred phase of neural firing within the M1 LFP cycle, relative to the LFP phase at peak movement speed. Data are for 98/125 (isometric task), 71/83 (free reaching), 61/78 (sleep), and 89/122 (sedation) neurons from M1/PMv, respectively. p values indicate the significance of the Rayleigh test of circular nonuniformity. Monkey R, open circles; monkey D, filled circles; monkey S, crosses. See also Figure S5.
Figure 8 Phase Locking of Neural Activity to the Cortical Cycle during Isometric Movement, Free Reaching, Natural Sleep, and Ketamine Sedation (A) Spike-triggered average LFP-PC trajectories for eight M1 neurons (blue) and six PMv neurons (red) over 200 ms before and after spike time (indicated by circles). Top row: averages of M1 LFPs; bottom row: averages of PMv LFPs. In all cases, the data are projected onto PC axes determined from the isometric task recordings. Nevertheless, a consistent rotational structure is observed across all behavioral states. See also Movie S5. (B) Summary of the preferred phase of neural firing within the M1 LFP cycle, relative to the LFP phase at peak movement speed. Data are for 98/125 (isometric task), 71/83 (free reaching), 61/78 (sleep), and 89/122 (sedation) neurons from M1/PMv, respectively. p values indicate the significance of the Rayleigh test of circular nonuniformity. Monkey R, open circles; monkey D, filled circles; monkey S, crosses. See also Figure S5.CC BY · PubMed Central

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  1. Berens, 2009, CircStat: a MATLAB toolbox for circular statistics, J. Stat. Softw., 31, 1

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Metadata

Authors
Hall, T. M., de Carvalho, F., & Jackson, A.
Affiliations
Newcastle University (GB)
Corresponding author
Jackson, Andrew
ORCID
Hall, Thomas M.
Venue
Neuron
Publisher
Elsevier BV
Published
2014-09
Volume
83
Issue
5
Pages
1185-1199
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2014.07.022
PMC
PMC4157580
OpenAlex
W2024591462
Cited by
134
References
49
Citations by year
2026: 4 · 2025: 7 · 2024: 8 · 2023: 13 · 2022: 15 · 2021: 14 · 2020: 10 · 2019: 18 · 2018: 12 · 2017: 12 · 2016: 10 · 2015: 10 · 2014: 1
FWCI
6.14
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Newcastle University ePrints (Newcastle Univesity) (cc-by)
Funders
  • Wellcome Trust (086561)
  • Medical Research Council (MR/K501396/1)
  • Engineering and Physical Sciences Research Council (EP/H051570/1)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
Keywords
primary motor cortex, premotor cortex, upper limb movement, ketamine sedation, sleep
MeSH terms
Animals, Biomechanical Phenomena, Electromyography, Female, Macaca mulatta, Models, Biological, Motor Cortex, Movement, Sleep, Procedural Sedation, Conscious Sedation, Nonlinear Dynamics, Upper Extremity

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