Extinction Interferes with the Retrieval of Visuomotor Memories Through a Mechanism Involving the Sensorimotor Cortex

Abstract

Savings is a fundamental property of learning. In motor adaptation, it refers to the improvement in learning observed when adaptation to a perturbation A (A1) is followed by re-adaptation to the same perturbation (A2). A common procedure to equate the initial level of error across sessions consists of restoring native sensorimotor coordinates by inserting null--unperturbed--trials (N) just before re-adaptation (washout). Here, we hypothesized that the washout is not innocuous but interferes with the expression of the new memory at recall. To assess this possibility, we measured savings following the A1NA2 protocol, where A was a 40° visual rotation. In Experiment 1, we increased the time window between N and A2 from 1 min to 24 h. This manipulation increased the amount of savings during middle to late phases of adaptation, suggesting that N interfered with the retrieval of A. In Experiment 2, we used repetitive TMS to evaluate if this interference was partly mediated by the sensorimotor cortex (SM). We conclude that the washout does not just restore the unperturbed sensorimotor coordinates, but inhibits the expression of the recently acquired visuomotor map through a mechanism involving SM. Our results resemble the phenomenon of extinction in classical conditioning.

The Influence of Movement Preparation Time on the Expression of Visuomotor Learning and Savings

“…We question the degree to which this bias effect can be considered a procedural memory of the kind that supports more complex and dynamic motor skills such as driving, juggling, or tying a shoelace. Therefore, contrary to widely held beliefs (Hikosaka et al, 2002;Doyon et al, 2003;Nguyen-Vu et al, 2013), cerebellumdependent learning (at least as it is currently understood) may play a fairly limited role in the acquisition of complex skills and instead might primarily serve to maintain calibration of existing skills (Telgen et al, 2014).…”

“…The component of adaptation expressed at low preparation times appears to resemble implicit, error-driven learning of the kind that appears to be supported by the cerebellum (Medina et al, 2001;Tseng et al, 2007;Taylor et al, 2014;Yang and Lisberger, 2014). Although this component of learning could be expressed at low preparation time, the only long-term memory it exhibited was a weak overall bias of reach direction on Day 2.…”

“…Learning in adaptation tasks is known to depend on an implicit , cerebellum-dependent (Tseng et al, 2007;Synofzik et al, 2008;Taylor et al, 2010;Izawa and Shadmehr, 2011) learning process that is posited to reflect updating of an internal forward model (Wolpert and Miall, 1996;Bastian, 2006;Izawa et al, 2012) driven by sensory prediction errors Tseng et al, 2007;Synofzik et al, 2008). In addition to this implicit, error-driven process, multiple additional processes are thought to contribute to learning in adaptation paradigms (Smith et al, 2006;Huang et al, 2011;Haith and Krakauer, 2013;Taylor and Ivry, 2014).…”

Electrifying the motor engram: effects of tDCS on motor learning and control

“…One could study patient populations with focal deficits in the cerebellum (Martin et al, 1996; Smith and Shadmehr, 2005; Donchin et al, 2011; Izawa et al, 2012), or the parietal cortex (Mutha et al, 2011), one could disrupt motor cortex function with transcranial magnetic stimulation (Muellbacher et al, 2002; Richardson et al, 2006; Hadipour-Niktarash et al, 2007; Censor et al, 2010; Orban de Xivry et al, 2011a; Villalta et al, 2013) or one could use functional brain imaging in healthy populations (Shadmehr and Holcomb, 1997; Della-Maggiore et al, 2009; Landi et al, 2011; Hardwick et al, 2012; Lohse et al, 2014). However, in the past decade a non-invasive method of investigation, transcranial direct current stimulation (tDCS; Priori et al, 1998; Nitsche and Paulus, 2000), has become increasingly popular, allowing for electrical modulation of the neural tissue in the living human brain, resulting in the ability to alter function of specific regions, providing possibilities in terms of accelerating learning and/or retention, as well as quantifying the contributions of each brain region to the process of motor learning.…”

Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

“…One important observation related to adaptation is that human subjects learn to adapt to a perturbation in fewer trials when they have previously experienced that perturbation, a phenomenon referred to as "savings" (Lackner and Lobovits 1977;Brashers-Krug et al 1996;Kojima et al 2004;Krakauer et al 2005;Zarahn et al 2008;Huang et al 2011;Villalta et al 2015).…”