TY - JOUR
T1 - Paradoxical Long-term Memory Augmentation following Temporal Pairing between "Limited" and "Extensive" Motor Sequence Training Experiences
AU - Oren, Yaniv
AU - Korman, Maria
AU - Karni, Avi
N1 - Publisher Copyright: © 2024 Massachusetts Institute of Technology. Published under a Creative Commons Attribution 4.0 International (CC BY 4.0) license.
PY - 2024/12/1
Y1 - 2024/12/1
N2 - Consecutive training on two movement sequences often leads to retroactive interference-obstructing memory for the initially trained sequence but not for the second. However, in the context of hippocampal-system dependent memories, a poor learning experience, memory for which would soon decay, can be enhanced if temporally paired with a "strong" memory triggering experience. The synaptic tagging and capture hypothesis explains this paradoxical enhancement by suggesting that only strong experiences generate cellular resources necessary for synaptic remodeling. However, synapses engaged in a "weak" learning experience can capture and utilize plasticity-related resources generated for a subsequent strong learning experience. Here, we tested whether such a "paradoxical" outcome would result in the context of motor (procedural) memory, if two movement sequences are unequally trained, consecutively. We show, in young adults (n = 100), that limited practice on a novel sequence of finger-to-thumb opposition movements led to different long-term outcomes, depending on whether and when (5 min, 5 hr) it was followed by extensive training on a different sequence. Five-minute pairing only resulted in overnight gains for the limited-trained sequence that were well-retained a week later; the overnight gains for the extensively trained sequence were compromised. Thus, consecutive training on different motor tasks can result in mnemonic interactions other than interference. We propose that the newly discovered mnemonic interaction provides the first-tier behavioral evidence in support of the possible applicability of notions stemming from the synaptic tagging and capture hypothesis in relation to human motor memory generation, specifically in relation to the practice-dependent consolidation of novel explicitly instructed movement sequences.
AB - Consecutive training on two movement sequences often leads to retroactive interference-obstructing memory for the initially trained sequence but not for the second. However, in the context of hippocampal-system dependent memories, a poor learning experience, memory for which would soon decay, can be enhanced if temporally paired with a "strong" memory triggering experience. The synaptic tagging and capture hypothesis explains this paradoxical enhancement by suggesting that only strong experiences generate cellular resources necessary for synaptic remodeling. However, synapses engaged in a "weak" learning experience can capture and utilize plasticity-related resources generated for a subsequent strong learning experience. Here, we tested whether such a "paradoxical" outcome would result in the context of motor (procedural) memory, if two movement sequences are unequally trained, consecutively. We show, in young adults (n = 100), that limited practice on a novel sequence of finger-to-thumb opposition movements led to different long-term outcomes, depending on whether and when (5 min, 5 hr) it was followed by extensive training on a different sequence. Five-minute pairing only resulted in overnight gains for the limited-trained sequence that were well-retained a week later; the overnight gains for the extensively trained sequence were compromised. Thus, consecutive training on different motor tasks can result in mnemonic interactions other than interference. We propose that the newly discovered mnemonic interaction provides the first-tier behavioral evidence in support of the possible applicability of notions stemming from the synaptic tagging and capture hypothesis in relation to human motor memory generation, specifically in relation to the practice-dependent consolidation of novel explicitly instructed movement sequences.
UR - http://www.scopus.com/inward/record.url?scp=85208049381&partnerID=8YFLogxK
U2 - https://doi.org/10.1162/jocn_a_02186
DO - https://doi.org/10.1162/jocn_a_02186
M3 - Article
C2 - 38739558
SN - 0898-929X
VL - 36
SP - 2807
EP - 2821
JO - Journal of Cognitive Neuroscience
JF - Journal of Cognitive Neuroscience
IS - 12
ER -