Learning the same motor task twice impairs its retention in a time- and dose-dependent manner

Abstract

Anterograde interference emerges when two differing tasks are learned in close temporal proximity, an effect repeatedly attributed to a competition between differing task memories. However, recent development alternatively suggests that initial learning may trigger a refractory period that occludes neuroplasticity and impairs subsequent learning, consequently mediating interference independently of memory competition. Accordingly, this study tested the hypothesis that interference can emerge when the same motor task is being learned twice, that is when competition between memories is prevented. In a first experiment, the inter-session interval (ISI) between two identical motor learning sessions was manipulated to be 2 min, 1 h or 24 h. Results revealed that retention of the second session was impaired as compared to the first one when the ISI was 2 min but not when it was 1 h or 24 h, indicating a time-dependent process. Results from a second experiment replicated those of the first one and revealed that adding a third motor learning session with a 2 min ISI further impaired retention, indicating a dose-dependent process. Results from a third experiment revealed that the retention impairments did not take place when a learning session was preceded by simple rehearsal of the motor task without concurrent learning, thus ruling out fatigue and confirming that retention is impaired specifically when preceded by a learning session. Altogether, the present results suggest that competing memories is not the sole mechanism mediating anterograde interference and introduce the possibility that a time- and dose-dependent refractory period—independent of fatigue—also contributes to its emergence. One possibility is that learning transiently perturbs the homeostasis of learning-related neuronal substrates. Introducing additional learning when homeostasis is still perturbed may not only impair performance improvements, but also memory formation.

Anterograde interference emerges along a gradient as a function of task similarity: A behavioural study

“…Retention, measured through reaching aftereffects, was evaluated immediately following adaptation in each learning session. Evidence of performance impairment upon the second learning session as compared with the first one would be assumed to be reflective of the emergence of anterograde interference, which has been previously observed as impaired relearning (Lerner et al, 2020) and/or retention capabilities (Hamel et al, 2021). This is also similar to the evaluation of retrograde interference (i.e., B → A → B), which can also be measured as impaired relearning (Brashers‐Krug et al, 1996; Krakauer, 2005; Wigmore et al, 2002) and/or retention capabilities (Keisler & Shadmehr, 2010; Pekny et al, 2011; Yan et al, 2020).…”

“…The most common interpretation for this phenomenon is that anterograde interference emerges because the memories of A and B compete for limited biological resources required for their encoding in functionally overlapping neural networks (Cantarero, Lloyd, & Celnik, 2013; Cantarero, Tang, et al, 2013; Herszage & Censor, 2018; Robertson, 2018). Although the notion that the memories of A and B share functionally overlapping networks appears consensual (Herszage & Censor, 2018; Robertson, 2018), recent work suggests that interference may not merely arise because of a competition between the two memories (Hamel et al, 2021).…”

“…In a series of experiments, Hamel et al (2021) had participants adapt to the same gradually introduced visual deviation twice over two distinct sessions (A → A) and measured retention levels through immediate reach aftereffect assessment. The results revealed that initial learning of A reliably interfered in a time‐, dose‐ and learning‐dependent manner by preventing the emergence of savings and by interfering with retention levels upon the second session as compared with the first one, indicative of the presence of anterograde interference.…”

“…Based on extensive neurobiological evidence (Keck, Hübener, et al, 2017; Kukushkin & Carew, 2017; Lee & Kirkwood, 2019; Smolen et al, 2016), one interpretation of the results from Hamel et al (2021) is that interference arises because the same neural networks—or largely overlapping ones—are recruited twice by the two identical learning sessions. Specifically, through the induction of synaptic plasticity, learning is known to transiently perturb the metabolic homeostasis of its associated neural network (Keck, Hübener, et al, 2017; Kukushkin & Carew, 2017; Lee & Kirkwood, 2019; Smolen et al, 2016).…”

“…In a fully within‐subject design meant to optimize statistical power (Algermissen & Mehler, 2018), right‐handed healthy participants ( n = 24) adapted twice to the same task that consisted of a gradually introduced ±21° visual deviation over two implicit learning sessions occurring in close temporal proximity (2 min; Hamel et al, 2021). Importantly, conditions were fully counterbalanced across participants to control for order effects (Brooks, 2012).…”