Learning to never forget-time scales and specificity of long-term memory of a motor skill

Abstract

Despite anecdotal reports that humans retain acquired motor skills for many years, if not a lifetime, long-term memory of motor skills has received little attention. While numerous neuroimaging studies showed practice-induced cortical plasticity, the behavioral correlates, what is retained and also what is forgotten, are little understood. This longitudinal case study on four subjects presents detailed kinematic analyses of humans practicing a bimanual polyrhythmic task over 2 months with retention tests after 6 months and, for two subjects, after 8 years. Results showed that individuals not only retained the task, but also reproduced their individual "style" of performance, even after 8 years. During practice, variables such as the two hands' frequency ratio and relative phase, changed at different rates, indicative of multiple time scales of neural processes. Frequency leakage across hands, reflecting intermanual crosstalk, attenuated at a significantly slower rate and was the only variable not maintained after 8 years. Complementing recent findings on neuroplasticity in gray and white matter, our study presents new behavioral evidence that highlights the multi-scale process of practice-induced changes and its remarkable persistence. Results suggest that motor memory may comprise not only higher-level task variables but also individual kinematic signatures.

Keywords: bimanual coordination; intermanual crosstalk; long-term memory; relative phase; retention; skill learning.

Figure 1

Apparatus and task. (A) Side and front view of the experimental setup. The dotted lines indicate enclosure, and the black objects on the floor of the enclosure indicate four microphones. The red dot at the wrist denotes the center of oscillation used for the calculation of the angular displacement of the pendulum. (B) Scheme of the schedule for practice and retention sessions.

Figure 2

Calculation of dependent variables. (A,B) Exemplary trial segment showing different movement patterns of two participants. The different peak alignments indicate the different phasing of the two hands. Frequency ratio and relative phase were calculated using methods described in the text. (C) The Euler form of the fast hand's angular displacement, ζ_F(t) = A_F(t)e^iϕ_F(t) where A_F and ϕ_F mean the amplitude and phase in the fast hand. The time series for two and a half cycles of the fast hand angle was taken from (B). (D) Instantaneous phase of both hands' position calculated with Hilbert transform. (E) Instantaneous frequency of slow and fast hand, ω_S and ω_F, calculated as time derivative of phase. Frequency ratio was the ratio of mean ω_F over ω_S (solid lines) in each trial. (F) Calculation of relative phase: phase of slow had ϕ_S multiplied by 3 is subtracted from phase of the fast hand ϕ_F. Mean and standard deviations across one trial served as dependent measures. (G) Exemplary power spectral densities of fast and slow hand in a single trial to illustrate the calculation of crosstalk. Fast hand crosstalk is the ratio of the two peaks in the fast hand (P₂/P₁), where P₁ is the primary peak and P₂ is the spectral power at the movement frequency of the slow hand. (H) Distance between two trajectories (normalized). For visualization purpose, the distance in the 3D space is shown by blue lines between corresponding points on the two trajectories.

Figure 3

Task-specific variables. (A–D) Frequency ratio (filled) and variability of relative phase (open) for each participant across 20 practice sessions and the 6-month (gray shade) and 8-year retention tests (yellow shade). Each data point is the average across three trials (5 points per session). The thin vertical lines indicate where the standard deviation of the frequency ratio in a moving window of 15 successive trials was 3 times greater than that of the last 10 sessions (moving from late to early trials).

Figure 4

Mean relative phase. (A,B) Mean relative phase of participants 1 and 2 across practice and at 6-month retention test and participants 3 and 4 including 8 years. (C) Pairwise comparison of individuals' relative phase between practice (last 10 sessions) and 6 months retention. AU: arbitrary unit. (D) Pairwise comparisons between 6-month and 8-year retention performance.

Figure 5

Actual movement frequency. (A–D) Mean fast (filled diamond) and slow (open circle) hand movement frequency in each participant (P1 to P4) over practice and retention. Gray shadows indicate one standard deviation.

Figure 6

Intermanual crosstalk. (A–D) Exemplary angular displacement profiles in the fast (brown) and slow (pink) hand of participant 4. In the middle of practice (A), accentuated peaks at every three cycles (arrows) were observed. At the end of practice and 6-month retention, accentuation disappeared (B,C). In an 8-year retention trial, the accentuated peaks (arrows) appeared again (D). (E–H) Learning and retention of intermanual crosstalk in each participant (P1 to P4). Crosstalk was log-transformed and fitted with a linear function: $\log \left[y(t)\right]=C-\frac{t}{\tau }$ The inverse slope parameter equals the time constant of change.

Figure 7

Average trajectories in four-dimensional state space. (A–D) Representation of average trajectories for each participant during the last practice session (thick black lines), 6-month retention (thick gray lines), and 8-year retention session (thin black lines). (E,F) Similarity between the trials of the last session, the 6-month retention trials and the 8-year retention trials of participants 3 and 4.