Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Abstract

The acquisition and execution of learned motor sequences are mediated by a distributed motor network, spanning cortical and subcortical brain areas. The sensorimotor striatum is an important cog in this network, yet how its two main inputs, from motor cortex and thalamus respectively, contribute to its role in motor learning and execution remains largely unknown. To address this, we trained rats in a task that produces highly stereotyped and idiosyncratic motor sequences. We found that motor cortical input to the sensorimotor striatum is critical for the learning process, but after the behaviors were consolidated, this corticostriatal pathway became dispensable. Functional silencing of striatal-projecting thalamic neurons, however, disrupted the execution of the learned motor sequences, causing rats to revert to behaviors produced early in learning and preventing them from re-learning the task. These results show that the sensorimotor striatum is a conduit through which motor cortical inputs can drive experiencedependent changes in subcortical motor circuits, likely at thalamostriatal synapses.

To move or to sense? Incorporating somatosensory representation into striatal functions

“…In one of the aforementioned time-estimation studies, a lesion of the primary motor cortex in naive rats prevented the learning of the embodied strategy but the same lesion was without effect when performed after learning. It was suggested that, during learning, the motor cortex provided a 'tutor' signal to subcorticals motor regions [60], most likely to the DLS [61]. In our general hypothesis, efference copy of motor programs and somatosensory responses would tutor DS SPN.…”

Basal forebrain cholinergic neurons selectively drive coordinated motor learning in mice

“…As we found that cholinergic inputs to both mPFC and motor cortex are required for coordinated motor acquisition, it is likely that cholinergic neuromodulation plays a critical role in the coactivation of mPFC-DMS and M1-DLS circuits during early stage rotarod learning (Kupferschmidt et al, 2017). As training progresses and instructional input from cortical projections is no longer driving experience-dependent refinement of striatal motor circuits (Wolff et al, 2019), cholinergic neuromodulation of cortical motor centers is no longer required. This is supported by our findings that ablation of cholinergic neurons after rotarod training elicited no effect on performance of the previously trained task.…”

Remembrance of things practiced with fast and slow learning in cortical and subcortical pathways

“…We shall show below that this is indeed the case. After developing the theory for this two-pathway model, we shall show in the following section that identifying the second input to striatum as thalamus provides an explanation for the asymmetric effects of motor cortical and thalamic lesions in rats described in the "Introduction" [28][29][30] .…”

“…In the case h = 0, on the other hand, the repeated pattern was not recalled accurately, illustrating that the input from the second pathway is necessary to protect practiced patterns from being overwritten. Thus, interpreting the two input pathways as cortical and thalamic inputs to striatum, the model accounts for the experimental observations in rodents that skilled behaviors and neural representations of kinematic variables are robust to the loss of cortical inputs [29][30][31] , but that such behaviors are not robust to the loss of thalamic input 28 . In summary, when an input pathway with fast supervised learning and another with slow Hebbian learning together drive a downstream population, the mechanisms of input alignment and control transfer enable the second input to gradually take over the role of the first in driving the downstream activity.…”

“…Recent lesion and inactivation experiments in rats have shown that sensorimotor striatum and its thalamic inputs are necessary for both learning and execution of a skilled lever-press sequence 28 . In the same task, however, input from motor cortex to striatum is necessary for learning the task, but not for performing the task once it has already been learned 28,29 . Furthermore, the representation of task-related kinematic variables in striatum during the task is similar in rats with and without cortical lesions 30 .…”