Formation of Long-Term Locomotor Memories Is Associated with Functional Connectivity Changes in the Cerebellar–Thalamic–Cortical Network

Abstract

Although motor adaptation is typically rapid, accumulating evidence shows that it is also associated with long-lasting behavioral and neuronal changes. Two processes were suggested to explain the formation of long-term motor memories: recall, reflecting a retrieval of previous motor actions, and faster relearning, reflecting an increased sensitivity to errors. Although these manifestations of motor memories were initially demonstrated in the context of adaptation experiments in reaching, indications of long-term motor memories were also demonstrated recently in other kinds of adaptation such as in locomotor adaptation. Little is known about the neural processes that underlie these distinct aspects of memory. We hypothesize that recall and faster relearning reflect different learning processes that operate at the same time and depend on different neuronal networks. Seventeen subjects performed a multisession locomotor adaptation experiment in the laboratory, together with resting-state and localizer fMRI scans, after the baseline and the locomotor adaptation sessions. We report a modulation of the cerebellar-thalamic-cortical and cerebellar-basal ganglia networks after locomotor adaptation. Interestingly, whereas thalamic-cortical baseline connectivity was correlated with recall, cerebellar-thalamic baseline connectivity was correlated with faster relearning. Our results suggest that separate neuronal networks underlie error sensitivity and retrieval components. Individual differences in baseline resting-state connectivity can predict idiosyncratic combination of these components.

Explicit Control of Step Timing During Split-Belt Walking Reveals Interdependent Recalibration of Movements in Space and Time

“…After-effects were computed as the averaged value for each gait parameter over the first thirty strides of post-adaptation. We used 30 strides, rather than only the initial 1–5 strides, because we were interested in characterizing long lasting after-effects (Long et al, 2015; Roemmich and Bastian, 2015; Mawase et al, 2017). We removed baseline biases from both measures by subtracting the baseline values for each gait parameter averaged over the last 40 strides during baseline (minus the very last transient 5 strides).…”

Chronic inflammation and apoptosis propagate in ischemic cerebellum and heart of non-human primates

“…Lesions affecting the anterior lobe vermal lobules I-III as well as posterior lobules VIII and IX can result in balance and gait instability [ 42 ]. Clinically, balance and gait disability are a common secondary condition following cerebral ischemia [ 44 - 53 ], and could potentially be reflected in the present observation of distal neurodegeneration in the cerebellum seen in our TGI NHPs.…”

“…A topographic study has revealed anatomical and functional hallmarks of specific cerebellar lobules [ 42 ]. Lobule III, a key component in the anterior lobe of the cerebellum, is predominantly responsible for leg and foot sensorimotor function [ 42 - 44 ]. Meanwhile, lobule IX is located in the posterior cerebellar lobe and functions in the visual guidance of movement, thereby utilizing visual information to direct movements and adjust reflexes appropriately [ 42 - 46 ].…”

Explicit control of step timing during split-belt walking reveals interdependent recalibration of movements in space and time

“…After-effects were computed as the averaged value for each gait parameter over the first thirty strides of post-adaptation. We used 30 strides, rather than only the initial 1 to 5 strides, because we were interested in characterizing long lasting after-effects (Long et al, 2015; Mawase et al, 2017; Roemmich and Bastian, 2015). We removed baseline biases from both measures by subtracting the baseline values for each gait parameter averaged over the last 40 strides during baseline (minus the very last transient 5 strides).…”