Gating of sensory input at spinal and cortical levels during preparation and execution of voluntary movement

Abstract

All bodily movements stimulate peripheral receptors that activate neurons in the brain and spinal cord through afferent feedback. How these reafferent signals are processed within the CNS during movement is a key question in motor control. We investigated cutaneous sensory-evoked potentials in the spinal cord, primary somatosensory and motor cortex, and premotor cortex in monkeys performing an instructed delay task. Afferent inputs from cutaneous receptors were suppressed at several levels in a task-dependent manner. We found two types of suppression. First, suppression during active limb movement was observed in the spinal cord and all three cortical areas. This suppression was induced by both bottom-up and top-down gating mechanisms. Second, during preparation for upcoming movement, evoked responses were suppressed exclusively in the motor cortical areas and the magnitude of suppression was correlated with the reaction time of the subsequent movement. This suppression could be induced by a top-down gating mechanism to facilitate the preparation and execution of upcoming movement.

Figures

Figure 1.

Methods. A, Nerve stimulation. Two nerve cuffs were implanted on the SR of the right arm: a distal bipolar cuff for stimulation (Stim) and a proximal tripolar cuff for recording volleys. Constant stimulus frequency (3 Hz) and current (2× threshold current, which activates the afferent fibers coding tactile stimuli) were used throughout the recording period. SR-evoked field potentials were recorded from both cervical spinal cord and cerebral cortex. Spinal SEPs were recorded within the gray matter of ipsilateral spinal cord and cortical SEPs were recorded in contralateral M1, PM, and S1 of wrist–arm representation. B, Behavioral task. Typical torque trace during a single flexion trial is shown with task epochs. Diagrams below depict the cursor controlled by the monkey (small filled square) and targets (larger squares) on video screen for the 10 epochs: first Rest, Cue, Delay, first RT, Active Move, Active Hold, second RT, Passive Move, second Rest, and Reward (for details, see Materials and Methods). C, Average of orthodromic volleys (n = 21,990) recorded in the proximal cuff electrodes. Gray shading represents the area of volleys measured for comparing them across the behavioral epochs. D, Area of orthodromic volley during behavioral task shown in B (22 flexion trials, 22 extension trials). Volleys were averaged separately for each behavioral epoch and areas plotted as percentage of rest.

Figure 2.

Measurement of SEPs. A, Measurement of onset latency (red arrow) and peak area (gray shading) of the SEPs. Stim, Time of stimulation of SR. Baselines (horizontal lines) were determined from mean of the background activity (20 ms before stimulation). Top, SEPs with preceding positive component (M1). Bottom, SEPs without preceding positive component. B, C, Penetration map of monkey M shown with onset latency (B) or the peak area (C). Largest SEPs in each penetration were analyzed. The latency and area was color-coded. D, E, Site in the cortex of monkey M (D) or monkey K (E) that were subjected to further comparison of the latency, area, and task-dependent modulation. Note that area 1 of S1 was not recorded in monkey K and data of monkey M were not subjected to the analysis of task-dependent modulation. “x” in E is the site where thumb extension movement was evoked by electrical stimulation with intracortical microstimulation (10 μA, 0.1 ms biphasic pulses, 10 pulses at 333 Hz).

Figure 3.

Example of SEPs. A, Typical examples of SR-evoked field potentials (averaged over all task epochs) in M1, S1, PM, and SC. Most recording sites had predominantly negative field potentials. This negative wave was followed by a positive component in S1 (red), and was sometimes preceded by a small positive component in M1 (dark blue) and PM (light blue). The negative field potentials probably reflect synaptic potentials in local neurons; the positive components could reflect recording of remote field potentials generated in adjacent regions. We analyzed the first negative component. B, Fields shown superimposed in faster sweeps. Triangles mark onset of the negative component. C, Locations of histologically confirmed sites where the recording shown in A and B was made. First, Transverse section of cervical spinal cord at C8 level. Second, Top view of cerebral cortex (left hemisphere). Third and fourth, Saggital sections made from the level shown in the top view (horizontal lines). Recordings from monkey M. ArS, Arcuate sulcus; IPS, intraparietal sulcus.

Figure 4.

Onset latency and area of SEPs. A, B, Means (±SD) of the onset latencies and areas of SR-evoked field potentials in monkeys M (A) and K (B). Individual recording sites for PM (n = 8 and 9), M1 (n = 7 and 11), and S1 (n = 6 and 11) are shown in Figure 2, D and E. Intraspinal recording sites (n = 29 and 8) are not shown. Onset latencies were shorter in SC and S1 than M1 and PM. *p < 0.01 (Tukey's test).

Figure 5.

Modulation of SEPs during task epochs. A, Example of a recording in a single trial (flexion). Field potentials were recorded simultaneously in the spinal cord and in the cerebral cortex (S1, PM, M1). Dashed lines indicate the timing of SR stimuli (Stim.) shown at bottom. PL, Palmaris longus; R, rest; C, cue; D, instructed delay; AM, active movement; H, hold; PM, passive movement. B, Three superimposed SR-evoked field potentials during rest (open circle), instructed delay (triangle), and active movement (filled circle). Note reduction of SEP during active movement. C, Epoch-dependent modulation of the area of SEPs evoked in M1, S1, PM, and SC. Data obtained in two monkeys (M1: n = 10 and 6, PM: n = 9 and 8, S1: n = 11 and 10, SC: n = 6 and 25; Fig. 2D,E); data in both flexion and extension trials were pooled and averaged.

Figure 6.

Modulation of SEPs during instructed delay and active movement. A, Averaged evoked potentials during rest (blue), delay (green), and active movement (red) periods in S1, M1, PM, and spinal cord. Note that SEPs were suppressed during active movement in all three cortical regions. SEPs were also suppressed during the instructed delay period in M1 and PM. B, Peak area of SEPs (shown in A) relative to movement onset. Example of extension trials. Mean ± SE of the peak area during control (rest period) are shown as the blue bars and dotted lines. Number of extension trials for obtaining each figure are given. *p < 0.05 from rest (Dunnet's test). C, The areas of evoked fields during rest, instructed delay period, and active movement period in SC, S1, M1, and PM. Data from two monkeys were pooled. *p < 0.05; ns, not significant (p ≥ 0.05) (t test).

Figure 7.

Modulation of SEPs during other behavioral periods. A, Comparison of the areas of SEPs between rest and sustained force period. SEPs of most regions were suppressed during sustained flexion and extension. *p < 0.05 (paired t test). B, Comparison between active and passive flexion (red) and extension (blue). *p < 0.05 (t test). Active extension (filled blue bar) induced greater suppression of SEPs than passive extension (open blue bar). C, Amplitude (angle) and speed (peak and mean) of active and passive movement are shown in both flexion and extension trials. Average of the trials used in B are shown. Mean ± SE. All differences within each kinematic parameter were significant (p < 0.01, Tukey's test).

Figure 8.

Relation between reaction times and SEP size during delay period. A, Torque traces for flexion (green) and extension (red) trials with short or long reaction times. Reaction times were measured from the go signal to the onset of flexion or extension torque. Average traces aligned on go signal were compiled separately for reaction times longer and shorter than the median. B, SR-evoked SEPs were compiled and averaged separately for stimuli applied during the instructed delay period before movements with fast and slow reaction times. Traces show examples of SEP in PM of monkey M. C, Means (±SD) of the area of SR-evoked SEPs evoked during the instructed delay periods before flexion trials with faster (light green) and slower (dark green) reaction time and extension trials with faster (red) and slower (brown) reaction time. D, Torque traces for flexion and extension trials. “Early” and “Late” represent the first and second half of the instructed delay period. E, SR-evoked SEPs were compiled and averaged separately for stimuli applied during early and late half of instructed delay period using same data as in A–C. F, Means (±SD) of the areas of SR-evoked SEPs evoked during early (green) or late (orange) part of instructed delay period. *p < 0.05; ns, not significant (p ≥ 0.05) (paired t test).

Figure 9.

Task-dependent correlations between SEPs. A, Amplitudes of SEPs during flexion (left) and extension (right) trials as a function of task. Areas of SEPs in SC, S1, M1, and PM (as percentage of rest) were averaged separately for task epochs. Open circles indicate a significant difference from rest (p < 0.05). B, Plots of the correlation coefficients for pairs of simultaneous trial-by-trial SEPs, as a function of task. Data from flexion and extension trials were combined. Correlations are shown for all combination of areas: SC, S1, M1, and PM. Significant (p < 0.01) covariance of SEPs during a given behavioral epoch is shown by open circles; filled circles indicate nonsignificant coefficient. Δr represents the depth of modulation (difference between the maximal and minimal r value during task). C, Cue; D, instructed delay; Act M, active movement; H, hold; Pass M, passive movement R, rest. C, Strength of covariance between the four recorded areas shown as no (dotted line), moderate (thin solid line), or strong (heavy line) correlation in each behavioral epoch.