Savings Upon Re-Aiming in Visuomotor Adaptation

Overview

Journal J Neurosci

Specialty Neurology

Date 2015 Oct 23

PMID 26490874

Citations 102

Authors

J Ryan Morehead

Salman E Qasim

Matthew J Crossley

Richard Ivry

Affiliations

Soon will be listed here.

Abstract

Significance Statement: Savings is the phenomenon in which people show faster relearning of a previously forgotten memory. In the motor learning domain, this phenomenon has been a puzzle for learning models that operate exclusively on error-based learning processes. We demonstrate, in a series of experiments, that savings selectively reflects improvements in action selection: Participants are more adept in invoking an appropriate aiming strategy when presented with a previously experienced perturbation. Indeed, improvements in action selection appear to be the sole source of savings in visuomotor adaptation tasks. We observe no evidence of savings in implicit error-based adaptation.

Citing Articles

Input device matters for measures of behaviour in online experiments.

Warburton M, Campagnoli C, Mon-Williams M, Mushtaq F, Morehead J Psychol Res. 2024; 89(1):29.

PMID: 39607544 PMC: 11604694. DOI: 10.1007/s00426-024-02065-1.

The cerebellum acts as the analog to the medial temporal lobe for sensorimotor memory.

Hadjiosif A, Gibo T, Smith M Proc Natl Acad Sci U S A. 2024; 121(42):e2411459121.

PMID: 39374383 PMC: 11494333. DOI: 10.1073/pnas.2411459121.

Fundamental processes in sensorimotor learning: Reasoning, refinement, and retrieval.

Tsay J, Kim H, McDougle S, Taylor J, Haith A, Avraham G Elife. 2024; 13.

PMID: 39087986 PMC: 11293869. DOI: 10.7554/eLife.91839.

Differential Aging Effects on Implicit and Explicit Sensorimotor Learning.

Cisneros E, Karny S, Ivry R, Tsay J bioRxiv. 2024; .

PMID: 39005271 PMC: 11244996. DOI: 10.1101/2024.07.02.601091.

Flexible multitask computation in recurrent networks utilizes shared dynamical motifs.

Driscoll L, Shenoy K, Sussillo D Nat Neurosci. 2024; 27(7):1349-1363.

PMID: 38982201 PMC: 11239504. DOI: 10.1038/s41593-024-01668-6.

References

Krakauer J, Ghez C, Ghilardi M . Adaptation to visuomotor transformations: consolidation, interference, and forgetting. J Neurosci. 2005; 25(2):473-8. PMC: 6725486. DOI: 10.1523/JNEUROSCI.4218-04.2005. View

Taylor J, Ivry R . Flexible cognitive strategies during motor learning. PLoS Comput Biol. 2011; 7(3):e1001096. PMC: 3048379. DOI: 10.1371/journal.pcbi.1001096. View

Pearson T, Krakauer J, Mazzoni P . Learning not to generalize: modular adaptation of visuomotor gain. J Neurophysiol. 2010; 103(6):2938-52. PMC: 2888232. DOI: 10.1152/jn.01089.2009. View

Huberdeau D, Haith A, Krakauer J . Formation of a long-term memory for visuomotor adaptation following only a few trials of practice. J Neurophysiol. 2015; 114(2):969-77. PMC: 4725125. DOI: 10.1152/jn.00369.2015. View

Wolpert D, Ghahramani Z, Jordan M . An internal model for sensorimotor integration. Science. 1995; 269(5232):1880-2. DOI: 10.1126/science.7569931. View

Mazzoni P, Krakauer J . An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci. 2006; 26(14):3642-5. PMC: 6674132. DOI: 10.1523/JNEUROSCI.5317-05.2006. View

Haith A, Huberdeau D, Krakauer J . The influence of movement preparation time on the expression of visuomotor learning and savings. J Neurosci. 2015; 35(13):5109-17. PMC: 6705405. DOI: 10.1523/JNEUROSCI.3869-14.2015. View

Lee J, Schweighofer N . Dual adaptation supports a parallel architecture of motor memory. J Neurosci. 2009; 29(33):10396-404. PMC: 2789989. DOI: 10.1523/JNEUROSCI.1294-09.2009. View

Zarahn E, Weston G, Liang J, Mazzoni P, Krakauer J . Explaining savings for visuomotor adaptation: linear time-invariant state-space models are not sufficient. J Neurophysiol. 2008; 100(5):2537-48. PMC: 2585408. DOI: 10.1152/jn.90529.2008. View

10.

Smith M, Ghazizadeh A, Shadmehr R . Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 2006; 4(6):e179. PMC: 1463025. DOI: 10.1371/journal.pbio.0040179. View

11.

Haruno M, Wolpert D, Kawato M . Mosaic model for sensorimotor learning and control. Neural Comput. 2001; 13(10):2201-20. DOI: 10.1162/089976601750541778. View

12.

Caithness G, Osu R, Bays P, Chase H, Klassen J, Kawato M . Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks. J Neurosci. 2004; 24(40):8662-71. PMC: 6729970. DOI: 10.1523/JNEUROSCI.2214-04.2004. View

13.

OLDFIELD R . The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971; 9(1):97-113. DOI: 10.1016/0028-3932(71)90067-4. View

14.

Krakauer J . Motor learning and consolidation: the case of visuomotor rotation. Adv Exp Med Biol. 2009; 629:405-21. PMC: 2672910. DOI: 10.1007/978-0-387-77064-2_21. View

15.

Herzfeld D, Vaswani P, Marko M, Shadmehr R . A memory of errors in sensorimotor learning. Science. 2014; 345(6202):1349-53. PMC: 4506639. DOI: 10.1126/science.1253138. View

16.

Huang V, Haith A, Mazzoni P, Krakauer J . Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron. 2011; 70(4):787-801. PMC: 3134523. DOI: 10.1016/j.neuron.2011.04.012. View

17.

Cunningham H, Welch R . Multiple concurrent visual-motor mappings: implications for models of adaptation. J Exp Psychol Hum Percept Perform. 1994; 20(5):987-99. DOI: 10.1037//0096-1523.20.5.987. View

18.

Orban de Xivry J, Lefevre P . Formation of model-free motor memories during motor adaptation depends on perturbation schedule. J Neurophysiol. 2015; 113(7):2733-41. PMC: 4416610. DOI: 10.1152/jn.00673.2014. View

19.

McDougle S, Bond K, Taylor J . Explicit and Implicit Processes Constitute the Fast and Slow Processes of Sensorimotor Learning. J Neurosci. 2015; 35(26):9568-79. PMC: 4571499. DOI: 10.1523/JNEUROSCI.5061-14.2015. View

20.

Medina J, Garcia K, Mauk M . A mechanism for savings in the cerebellum. J Neurosci. 2001; 21(11):4081-9. PMC: 6762711. View