Whole-brain dynamics of human sensorimotor adaptation

Abstract

Individuals exhibit differences in learning ability, but the reasons for these differences are unclear. We used human functional magnetic resonance imaging (fMRI) to show that dynamic changes in whole-brain networks during the early stages of sensorimotor adaptation predict patterns of learning that emerge across two days of learning and relearning. A clustering of participant behavioural data revealed three distinct profiles of learners: individuals who learned quickly on both days, individuals who learned slowly on both days, and individuals who learned slowly on the first day, but quickly on the second day. These learning profiles were associated with the degree of modular reconfiguration during early learning on the first day, and with the selective recruitment of a cognitive network of regions, including areas in anterior temporal and prefrontal cortex. These findings demonstrate that across-day profiles of adaptation can be traced to whole-brain dynamics that manifest during initial learning.

Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation

“…Since a full characterization of subject performance would require summarizing rates of learning, unlearning, and the total adaptation on both days (along with other features of performance, e.g., reaction times, which have been linked to distinct cognitive or motor processes), here we sought an interpretable, low-dimensional summary amenable to simple statistical analysis. This approach was motivated by our observation that standard summary measures generally failed to capture overall performance patterns across both days (see also Standage et al, 2020 ). For example, ‘savings’, the difference in early learning performance across days, failed to distinguish between subjects who learned the rotation rapidly on both days versus those who learned and relearned slowly.…”

Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation

“…Note that the aforementioned procedure, repeated over two fMRI sessions, was collected to explore individual differences in functional brain organization related to sensorimotor adaptation, de-adaptation, and subsequent re-adaptation (see [57, 87]). Given that the present study aims to specifically examine changes in functional brain architecture during initial adaptation to a novel visuomotor perturbation, we focused our analyses exclusively on the task scans of the first session.…”

Fundamental processes in sensorimotor learning: Reasoning, Refinement, and Retrieval

“…Various forms of feedback and sensorimotor experiences, such as motor error, reward, and movement repetition, have traditionally been thought to induce implicit learning (Doya, 2000;Izawa & Shadmehr, 2011;Pascual-Leone et al, 1993;Shadmehr et al, 2010). Moreover, these forms of implicit learning are believed to depend on separable neural pathways: Error-based motor learning engages cerebellar-cortical interactions (Marr, 1969), reinforcement-based learning engages basal ganglia-cortical interactions (Schultz et al, 1997), and use-dependent learning (i.e., learning driven by simple movement repetition) modulates neural tuning curves in primary sensorimotor areas (Classen et al, 1998) (also see: (Areshenkoff et al, 2023;Nick et al, 2023;Standage et al, 2022)). In this section, we discuss studies that have challenged the view that sensorimotor learning is solely implicit, demonstrating that performance on a broad range of simple motor learning tasks can be largely driven by the deployment of an explicit strategy.…”