Mechanistic determinants of effector-independent motor memory encoding

Abstract

<jats:p>Coordinated, purposeful movements learned with one effector generalize to another effector, a finding that has important implications for tool use, sports, performing arts, and rehabilitation. This occurs because the motor memory acquired through learning comprises representations that are effector-independent. Despite knowing this for decades, the neural mechanisms and substrates that are causally associated with the encoding of effector-independent motor memories remain poorly understood. Here we exploit intereffector generalization, the behavioral signature of effector-independent representations, to address this crucial gap. We first show in healthy human participants that postlearning generalization across effectors is principally predicted by the level of an implicit mechanism that evolves gradually during learning to produce a temporally stable memory. We then demonstrate that interfering with left but not right posterior parietal cortex (PPC) using high-definition cathodal transcranial direct current stimulation impedes learning mediated by this mechanism, thus potentially preventing the encoding of effector-independent memory components. We confirm this in our final experiment in which we show that disrupting left PPC but not primary motor cortex after learning has been allowed to occur blocks intereffector generalization. Collectively, our results reveal the key mechanism that encodes an effector-independent memory trace and uncover a central role for the PPC in its representation. The encoding of such motor memory components outside primary sensorimotor regions likely underlies a parsimonious neural organization that enables more efficient movement planning in the brain, independent of the effector used to act.</jats:p>

Evidence for an effector-independent action system from people born without hands

“…The ability to transfer motor skills from a trained effector to a novel effector indicates that movements are represented not only in terms of specific muscle patterns, but also in more abstract forms that can be flexibly translated into alternative muscle patterns. Consistent with our findings, such learning transference relies on the frontal motor areas and parietal lobe (96,99,104). Whereas these domains differ in time scale, from evolutionarily old (e.g., grasping) to more recent (e.g., writing) and to newly-trained visuomotor perturbations, studies on different domains indicate that effector-independent motor representation may be a common mechanism that supports flexible motor execution and learning across effectors.…”

Dissociable mechanistic contributions of limb and task related errors during human sensorimotor learning

“…The distinction between SPE-and TE-sensitive mechanisms suggests that they might also be neurally separable. While SPE-based learning depends on the cerebellum (Galea et al, 2011;Martin et al, 1996;Morehead et al, 2017;Tseng et al, 2007) and parietal cortex (Kumar et al, 2020;Mutha et al, 2011aMutha et al, , 2011bMutha et al, , 2017, the presence of a TE is known to activate reward-sensitive cortico-striatal pathways (Diedrichsen et al, 2005;Inoue et al, 2016). Failure to obtain reward could trigger re-aiming via mental rotation or other processes dependent on M1 and premotor cortex (Georgopoulos & Massey, 1987;Georgopoulos et al, 1989;Kosslyn et al, 1998;Tomasino et al, 2005).…”

“…Understanding how we adapt our movements to such changes has been of tremendous interest in sensorimotor neuroscience. Laboratory tasks often simulate such conditions using various visual (Krakauer, 2009; Kumar et al, 2020; Martin et al, 1996; Morehead et al, 2017; Wang & Sainburg, 2005) or dynamic (Dizio and Lackner, 1995; Kumar et al, 2019; Sainburg et al, 1999; Shadmehr and Mussa-Ivaldi, 1994; Sing et al, 2009) perturbations that not only induce a discrepancy in the expected versus actual sensory feedback (sensory prediction error, SPE), but can also result in a failure to achieve the task goal (task error, TE). It is generally believed that SPEs are compensated via implicit updates to internal neural representations that define the relationship between movement commands and their sensory consequences.…”

Previous motor actions outweigh sensory information in sensorimotor learning

“…The two different task contexts we investigated in this work are distinct to previous studies, as we did not test generalization from one effector to another, such as performing a task with the right hand and switching to the left [11,21], or switching from a motor to a perceptual task [16]. Instead, our two contexts represent two distinct cue-action mappings, though performed with the same modality (oculomotor system).…”