Gone in 0.6 seconds: the encoding of motor memories depends on recent sensorimotor states

Abstract

Real-world tasks often require movements that depend on a previous action or on changes in the state of the world. Here we investigate whether motor memories encode the current action in a manner that depends on previous sensorimotor states. Human subjects performed trials in which they made movements in a randomly selected clockwise or counterclockwise velocity-dependent curl force field. Movements during this adaptation phase were preceded by a contextual phase that determined which of the two fields would be experienced on any given trial. As expected from previous research, when static visual cues were presented in the contextual phase, strong interference (resulting in an inability to learn either field) was observed. In contrast, when the contextual phase involved subjects making a movement that was continuous with the adaptation-phase movement, a substantial reduction in interference was seen. As the time between the contextual and adaptation movement increased, so did the interference, reaching a level similar to that seen for static visual cues for delays >600 ms. This contextual effect generalized to purely visual motion, active movement without vision, passive movement, and isometric force generation. Our results show that sensorimotor states that differ in their recent temporal history can engage distinct representations in motor memory, but this effect decays progressively over time and is abolished by ∼600 ms. This suggests that motor memories are encoded not simply as a mapping from current state to motor command but are encoded in terms of the recent history of sensorimotor states.

Figure 1.

Experimental paradigm. A, The subject grasps the handle of the robotic manipulandum (vBOT) while seated. Visual feedback of movements is presented veridically using a top-mounted computer screen viewed via a mirror. The subject's forearm is fixed to the handle and supported by an air sled. B, Workspace layout of the experiment. There were four possible cue locations (gray circles, C1–C4), one central target (green circle; note that in the experiment this was displayed as gray), and four final targets (yellow circles, T1–T4). C, Table of the force-field directions as a function of cue and target location. During the exposure phase of the experiments, force fields were applied on the subjects' hands by the robot as the subject performed a movement between the central location and the final target. The force field applied—CW or CCW—depended on both the target direction (0°, 90°, 180°, and 270°) and the cue location (45°, 135°, 225°, and 315°), but not every combination was used. For each target location, two possible cue locations could be chosen (one for each force-field direction) corresponding to ±135° relative angle around the central target. Only the combination of the cue location and final target location specified the force-field direction. In a block of trials, all cue locations and final target locations were pseudorandomly presented such that CW and CCW trials were mixed equally. The table shows the association of force field and cue–target location used in half the subjects for a given experiment. In the other half, the association was reversed.

Figure 2.

Static visual cue experiments. A, Experimental design. Subjects started the trial with their hand at the central location (green circle) while both the cue location (gray circle) and final target (yellow circle) were visually presented. Movement initiation was either signified by an acoustic beep (static visual cue condition) or the cue color changing from gray to white (static visual cue attention experiment). The combination of cue (e.g., C3) and target (e.g., T1) uniquely specified the CW force field (Fig. 1B), applied once the subjects initiated the movement to the final target. B, For the same final target (T1), if cue C2 was visually presented to the subjects, this uniquely specified the CCW force field, applied once the movement was initiated. C, MPE plotted against block number. The mean across all subjects (solid line) and SE across subjects (shaded region) for each block in both the static visual cue (blue) and static visual cue attention (navy blue) experiments are shown. Although the two force fields produce error in the opposite directions, the sign of errors on trials on which the CCW field was presented have been reversed so that all errors in the direction of the force field are shown as positive. On block 13, the two curl fields were introduced (exposure, gray shaded region), which remained on until block 89, when subjects returned to the null force field. D, Percentage force compensation computed from clamp trials throughout the experiment. The mean ± SE force across subjects over two blocks is plotted as a percentage of the force required for estimated complete compensation. Gray shaded region indicates exposure blocks in which the curl force fields were applied.

Figure 3.

Hand paths during the movements between the central location (green circle) and final target (yellow circle) for the static visual cue and dwell time experiments. The mean (solid line), SE (dark shaded region), and SD (light shaded region) across all subjects for each condition are plotted. The trials on which the CW force field was applied are shown in red, and the trials in which the CCW force field was applied are shown in blue. Pre-exposure, The mean of the last eight trials in the initial null field (block 12). Initial exposure, The first eight trials in the curl force fields (block 13). Final exposure, The last eight trials in the curl field (block 88). Post exposure, The first eight trials in the null field during the washout (aftereffect trials) (block 89). Trials in which the force field is applied are shown with the shaded gray background. A, Paths in the visual static condition. B, Paths in the 1000 ms dwell condition. C, Paths in the 500 ms dwell condition. D, Paths in the 150 ms dwell condition. E, Paths in the 0 ms dwell condition.

Figure 4.

Dwell time contextual effect experiments. A, Experimental design. In the contextual phase, subjects moved from the cue location to the central target while the final target was visually displayed. No forces were applied during this movement at any stage of the experiment. Subjects were then required to remain in the central location for a set dwell time (0, 150, 500, or 1000 ms). After remaining in the central target for the correct time, subjects moved to the final target. The curl force fields were applied during this phase of the trial. For example, the movement from cue C3 and to target T1 uniquely specified the CW force field. B, The movement from cue C2 and to final target T1 uniquely specified the CCW force field. C, Speed profiles for the single force-field condition (black) and dwell time conditions of 0 ms (red), 150 ms (yellow), 500 ms (green), and 1000 ms (cyan) aligned on the contextual movement initiation. The mean and SE of the hand speed profiles are shown across all subjects. D, Speed profiles for the single force-field condition (black) and the dwell time conditions of 0 ms (red), 150 ms (yellow), 500 ms (green), and 1000 ms (cyan) aligned on the peak velocity of the second movement. The mean and SE of the hand speed profiles are shown across all subjects. E, Mean hand path error (MPE) and SE as a function of block, averaged across all subjects for dwell times of 0, 150, 500, and 1000 ms as well as for the single force-field condition (black dashed line). Shaded region indicates exposure blocks in which the curl force fields were applied. Each block in the single force-field condition consisted of nine trials (8 force-field trials and 1 clamp trial) and consecutive blocks were averaged together. This provides an even comparison across blocks with all other experimental conditions as the identical number of force-field trials (of any one field direction) are presented in a block. F, Percentage force compensation computed from clamp trials throughout the experiment. The mean ± SE force over two blocks across subjects is plotted as a percentage of the force required for estimated complete compensation, for dwell times of 0 ms (red), 150 ms (yellow), 500 ms (green), and 1000 ms (cyan), as well as the corresponding values for the single force-field condition (black dashed). Shaded region indicates exposure blocks in which the curl force fields were applied.

Figure 5.

Motion before contextual information cues learning. A, Experimental design. The contextual phase comprised two components. Prior movement, The first movement (cue location to central target) occurred before the complete contextual information (presentation of target), which determined the force-field direction. The trial was initiated with the subject's hand at one of the cue locations (C3 in this case) while the central location was visually presented. The subject then moved to the central location. Target appearance, Once the subject was within the central location, the target appeared. Adaptation phase, Subjects then moved to the final target, and the force field was applied as soon as subjects initiated the movement. In this case, the previous movement from cue C3 combined with the current target presentation of T1 specified the CW force field. B, The identical previous movement from cue C3 to the central target was performed. However, in the target appearance phase, target T2 was presented. This combination specified the CCW force field on the adaptation phase of the movement. C, Mean MPE (green trace) and SE (green shaded region) across all subjects and blocks during the motion before contextual presentation experiment. For comparison, the mean results for the static visual (blue trace) and 0 ms dwell time (red trace) conditions are shown. Shaded gray region indicates the exposure period in which the two curl force fields were applied. D, Percentage force compensation computed from clamp trials throughout the experiment. The mean ± SE force over two blocks across subjects is plotted as a percentage of the force required for estimated complete compensation. For comparison, the mean results for the static visual normal (blue trace) and 0 ms dwell time (red trace) conditions are shown. Shaded region indicates exposure blocks in which the curl force fields were applied.

Figure 6.

Sensorimotor cues involved in contextual effects. In all conditions, to aid comparison, the mean results for the normal condition static visual (blue trace) and 0 ms dwell time (red trace) conditions are shown on both MPE and force compensation plots. Shaded gray region indicates exposure period in which the two curl force fields were applied. A, MPE in the dynamic visual context condition. The mean MPE (purple trace) and SE (purple shaded region) across all subjects, as a function of experimental block. In this condition, the cursor was moved visually from the cue location to the central location while the subject's hand was stationary at the central location before the subject actively moved to the final target. B, Percentage force compensation in the dynamic visual condition. C, MPE in the dynamic visual context with eye fixation. Subjects were required to maintain eye fixation at the central target during the dynamic visual presentation. D, Percentage force compensation in the dynamic visual context with eye fixation. E, MPE in the active previous motion with no visual cursor condition. F, Percentage force compensation in the active previous motion with no visual cursor condition. G, MPE in the passive previous motion with no visual cursor condition. H, Percentage force compensation in the passive previous motion with no visual cursor condition. I, MPE in the isometric force context condition. J, Percentage force compensation in the isometric force context condition.

Figure 7.

Contextual effects vary with dwell time. A, The mean ± SE force on clamp trials (in direction toward target T1) as a percentage of the force required for estimated complete compensation. Values for all experiments (on the last third of trials during force-field exposure) are plotted as a function of the mean dwell time that subjects used in these conditions, with SE indicated by horizontal error bars. Note that most of the horizontal error bars are so small that they disappear under the symbols. For comparison, the results from the visual static conditions are plotted as a line (shaded region indicates SE) across all dwell times, because they are not related to a particular dwell time. B, The mean ± SE MPE over the last block of trials during force-field exposure. C, The mean ± SE MPE over the first block of trials in the postexposure session in all experiments. D, The mean ± SE peak velocity across all subjects in all experimental conditions experiments (on the last third of trials during force-field exposure), plotted as a function of dwell time.