Manipulation of peripheral neural feedback loops alters human corticomuscular coherence

Abstract

Sensorimotor EEG shows approximately 20 Hz coherence with contralateral EMG. This could involve efferent and/or afferent components of the sensorimotor loop. We investigated the pathways responsible for coherence genesis by manipulating nervous conduction delays using cooling. Coherence between left sensorimotor EEG and right EMG from three hand and two forearm muscles was assessed in healthy subjects during the hold phase of a precision grip task. The right arm was then cooled to 10 degrees C for approximately 90 min, increasing peripheral motor conduction time (PMCT) by approximately 35% (assessed by F-wave latency). EEG and EMG recordings were repeated, and coherence recalculated. Control recordings revealed a heterogeneous subject population. In 6/15 subjects (Group A), the corticomuscular coherence phase increased linearly with frequency, as expected if oscillations were propagated along efferent pathways from cortex to muscle. The mean corticomuscular conduction delay for intrinsic hand muscles calculated from the phase-frequency regression slope was 10.4 ms; this is smaller than the delay expected for conduction over fast corticospinal pathways. In 8/15 subjects (Group B), the phase showed no dependence with frequency. One subject showed both Group A and Group B patterns over different frequency ranges. Following cooling, averaged corticomuscular coherence was decreased in Group A subjects, but unchanged for Group B, even though both groups showed comparable slowing of nervous conduction. The delay calculated from the slope of the phase-frequency regression was increased following cooling. However, the size of this increase was around twice the rise in PMCT measured using the F-wave (regression slope 2.33, 95% confidence limits 1.30-3.36). Both afferent and efferent peripheral nerves will be slowed by similar amounts following cooling. The change in delay calculated from the coherence phase therefore better matches the rise in total sensorimotor feedback loop time caused by cooling, rather than just the change in the efferent limb. A model of corticomuscular coherence which assumes that only efferent pathways contribute cannot be reconciled to these results. The data rather suggest that afferent feedback pathways may also play a role in the genesis of corticomuscular coherence.

Figure 1. Change in F-wave latency during arm cooling in a single subject

A, F-waves elicited by stimulation of the median nerve at the wrist at different times after the onset of cooling. Each trace shows 30–40 superimposed sweeps. M-wave clipped for clarity. Arrowheads mark the 10th percentile F-wave onset latency. STIM, point of stimulus delivery. B and C, histograms of F-wave latency at the start (B) and end (C) of cooling. Arrowheads indicate the 10th percentile of the latency distribution. D, 10th percentile of F-wave latency plotted against time after cooling onset. Subject 2tt.

Figure 2. Intrinsic hand muscles and forearm muscles were affected differently by cooling

A and B, average force produced by electrical stimulation of an intrinsic hand muscle (A, 1DI, direct stimulation over belly of muscle) and a forearm muscle (B, FDS, stimulation of median nerve at cubital fossa). Thin lines, control data; thick lines, after cooling. Arrowheads denote points of maximum force used for twitch time measurement. n = 22–39 stimuli. Subject 8cnr. C, M-wave duration increased only marginally following cooling. STIM, point of stimulus delivery to median nerve at the wrist. Thin lines, control data; thick lines, after cooling. Subject 2tt. D and E, power spectra of unrectified EMG from intrinsic hand muscles (D) and forearm muscles (E). Spectra are averaged across all muscles and subjects: n = 45 for intrinsic hand muscles and n = 30 for forearm muscles.

Figure 3. Phase slope grouping method

Plots (A–C) are single-subject examples of coherence phase versus frequency. Phase estimates from each of the three intrinsic hand muscles have been superimposed. Each point is plotted three times at phases separated by 2π radians, to allow linear trends to be visualized across cycle boundaries. Points are only shown for frequencies with significant coherence. Error bars show 95% confidence limits. Broken lines show linear regression fit. A, subject 2rd, with a phase–frequency regression slope significantly different from zero. B, subject 8cnr with regression slope not significantly different from zero. C, subject 2kb showed a zero-slope relationship for low frequencies of coherence, but a significantly non-zero slope at higher frequencies. D, histogram of delays between EEG and EMG calculated from regression slopes in all subjects. Positive delays indicate EEG leads EMG. Black bars show slopes significantly different from zero.

Figure 4. Single-subject examples of coherence changes after cooling

A, C and E, coherence spectra averaged across the three intrinsic hand muscles recorded; B, D and E, coherence averaged across the two forearm muscles recorded. A and B, Group A subject 2rd. C and D, Group B subject 8cnr. E and F, anomalous subject 2kb, not classified into either group. In all plots, thin lines show control, thick lines show cold data. Grey shading marks bins where control and cold spectra were significantly different (P < 0.05). Coherence below the broken line is not significantly different from zero.

Figure 5. The effect of arm cooling on EEG and EMG power spectra averaged across subjects in each group

A–C, EEG power. D–F, full-wave-rectified EMG power averaged over intrinsic hand muscles. G–I, full-wave-rectified EMG power averaged over forearm muscles. A, D, G, Group A subjects. B, E, H, Group B subjects. C, F, I, anomalous subject not classified into either group. In all panels, thin line shows control data with arm warm; thick line after cooling. Grey shading marks bins where cooling significantly changes the measure (P < 0.05).

Figure 6. Coherence changes following arm cooling averaged across subjects in each group

A, C and E, data averaged across intrinsic hand muscles; B, D and E, data averaged across forearm muscles. A and B, Group A subjects. C and D, Group B subjects. E and F, anomalous subject not classified into either group. Same plotting conventions as in Fig. 5. Coherence below the broken line is not significantly different from zero.

Figure 7. Changes in coherence phase after cooling

A, Group A subject 2rd. B, Group B subject 8cnr. C, anomalous subject 2kb. Phase plotting conventions as in Fig. 3A–C. ○, control data; •, after cooling. D, change in phase delay plotted versus change in peripheral motor conduction time (PMCT) following arm cooling. Phase delay was calculated from the difference in coherence phase–frequency regression slopes using intrinsic hand muscles. PMCT was measured from the AbPB muscle. Each point represents one subject. Error bars show 95% confidence limits, calculated from the confidence limits on the regression slopes. Broken line shows a linear regression fit constrained to intersect the origin.