Neural Substrates Related to Motor Memory with Multiple Timescales in Sensorimotor Adaptation

Kim, Sung Shin; Ogawa, Kazuhiko; Lv, Jinchi; Schweighofer, Nicolas; Imamizu, Hiroshi

doi:10.1371/journal.pbio.1002312

“…The cerebellar-thalamic tract of the superior cerebellar peduncle connect the cerebellar hemisphere to the contralateral thalamus, which in turn projects to areas in the motor cortex (Sakai et al, 2002;Jeljeli et al, 2003;Stepniewska et al, 2003). Previous brain stimulation (Galea et al, 2011;Jayaram et al, 2012), neuroimaging (Albert et al, 2009b;Vahdat et al, 2011;Della-Maggiore et al, 2015a;Kim et al, 2015;Villalta et al, 2015), and lesions studies (Chen et al, 2006;Reisman et al, 2007;Tseng et al, 2007;Choi et al, 2009;Xu-Wilson et al, 2009) provide evidence for the critical involvement of the nodes of this network in motor learning. Consistent with our observation, Chen et al (2006) found that disrupting the cerebellar-thalamic pathway either by deep brain stimulation or by thalamotomy largely impaired the ability to adapt to external perturbation.…”

Section: Connectivity Modulation In the Cerebellar-thalamic-cortical mentioning

confidence: 96%

“…Alternatively, these changes may reflect long-term changes in connectivity. In that case, the inconsistency between the large-scale connectivity changes (Della-Maggiore and McIntosh, 2005;Debas et al, 2010;Della-Maggiore et al, 2015b) and the narrow generalization that is typically reported in adaptation learning (Krakauer et al, 2000) may suggest that the connectivity changes are driven by a selective ensemble of neurons in each region.…”

Section: Baseline Connectivity Reflects An Idiosyncratic Combination mentioning

confidence: 99%

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

Mawase¹,

Bar-Haim²,

Shmuelof

³

2016

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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.

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“…Alternatively, these changes may reflect long-term changes in connectivity. In that case, the inconsistency between the large-scale connectivity changes (Della-Maggiore and McIntosh, 2005;Debas et al, 2010;Della-Maggiore et al, 2015b) and the narrow generalization that is typically reported in adaptation learning (Krakauer et al, 2000) may suggest that the connectivity changes are driven by a selective ensemble of neurons in each region.…”

Section: Baseline Connectivity Reflects An Idiosyncratic Combination mentioning

confidence: 99%

“…The cerebellar-thalamic tract of the superior cerebellar peduncle connect the cerebellar hemisphere to the contralateral thalamus, which in turn projects to areas in the motor cortex (Sakai et al, 2002;Jeljeli et al, 2003;Stepniewska et al, 2003). Previous brain stimulation (Galea et al, 2011;Jayaram et al, 2012), neuroimaging (Albert et al, 2009b;Vahdat et al, 2011;Della-Maggiore et al, 2015a;Kim et al, 2015;Villalta et al, 2015), and lesions studies (Chen et al, 2006;Reisman et al, 2007;Tseng et al, 2007;Choi et al, 2009;Xu-Wilson et al, 2009) provide evidence for the critical involvement of the nodes of this network in motor learning. Consistent with our observation, Chen et al (2006) found that disrupting the cerebellar-thalamic pathway either by deep brain stimulation or by thalamotomy largely impaired the ability to adapt to external perturbation.…”

Section: Connectivity Modulation In the Cerebellar-thalamic-cortical mentioning

confidence: 99%

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

Mawase¹,

Bar-Haim²,

Shmuelof³

2017

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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.

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“…Some of these investigations also showed that after an initial increase in cerebellar activity there is a decrease of activation over time11121314. However, other studies also implicated the CB in retention or later phases of learning151617181920.…”

mentioning

confidence: 99%

Temporal dynamics of cerebellar and motor cortex physiological processes during motor skill learning

Spampinato

¹

,

Celnik²

2017

Sci Rep

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Learning motor tasks involves distinct physiological processes in the cerebellum (CB) and primary motor cortex (M1). Previous studies have shown that motor learning results in at least two important neurophysiological changes: modulation of cerebellar output mediated in-part by long-term depression of parallel fiber-Purkinje cell synapse and induction of long-term plasticity (LTP) in M1, leading to transient occlusion of additional LTP-like plasticity. However, little is known about the temporal dynamics of these two physiological mechanisms during motor skill learning. Here we use non-invasive brain stimulation to explore CB and M1 mechanisms during early and late motor skill learning in humans. We predicted that early skill acquisition would be proportional to cerebellar excitability (CBI) changes, whereas later stages of learning will result in M1 LTP-like plasticity modifications. We found that early, and not late into skill training, CBI changed. Whereas, occlusion of LTP-like plasticity over M1 occurred only during late, but not early training. These findings indicate a distinct temporal dissociation in the physiological role of the CB and M1 when learning a novel skill. Understanding the role and temporal dynamics of different brain regions during motor learning is critical to device optimal interventions to augment learning.

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Neural Substrates Related to Motor Memory with Multiple Timescales in Sensorimotor Adaptation

Cited by 95 publications

References 65 publications

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

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

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

Temporal dynamics of cerebellar and motor cortex physiological processes during motor skill learning

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