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. 2017 Mar 1;37(9):2377-2386.
doi: 10.1523/JNEUROSCI.2511-16.2017. Epub 2017 Jan 30.

Cerebellar-M1 Connectivity Changes Associated with Motor Learning Are Somatotopic Specific

Danny A Spampinato  1   2   3 , Hannah J Block  4   5 , Pablo A Celnik  6   2   3
Affiliations

Cerebellar-M1 Connectivity Changes Associated with Motor Learning Are Somatotopic Specific

Danny A Spampinato et al. J Neurosci. .

Abstract

One of the functions of the cerebellum in motor learning is to predict and account for systematic changes to the body or environment. This form of adaptive learning is mediated by plastic changes occurring within the cerebellar cortex. The strength of cerebellar-to-cerebral pathways for a given muscle may reflect aspects of cerebellum-dependent motor adaptation. These connections with motor cortex (M1) can be estimated as cerebellar inhibition (CBI): a conditioning pulse of transcranial magnetic stimulation delivered to the cerebellum before a test pulse over motor cortex. Previously, we have demonstrated that changes in CBI for a given muscle representation correlate with learning a motor adaptation task with the involved limb. However, the specificity of these effects is unknown. Here, we investigated whether CBI changes in humans are somatotopy specific and how they relate to motor adaptation. We found that learning a visuomotor rotation task with the right hand changed CBI, not only for the involved first dorsal interosseous of the right hand, but also for an uninvolved right leg muscle, the tibialis anterior, likely related to inter-effector transfer of learning. In two follow-up experiments, we investigated whether the preparation of a simple hand or leg movement would produce a somatotopy-specific modulation of CBI. We found that CBI changes only for the effector involved in the movement. These results indicate that learning-related changes in cerebellar-M1 connectivity reflect a somatotopy-specific interaction. Modulation of this pathway is also present in the context of interlimb transfer of learning.SIGNIFICANCE STATEMENT Connectivity between the cerebellum and motor cortex is a critical pathway for the integrity of everyday movements and understanding the somatotopic specificity of this pathway in the context of motor learning is critical to advancing the efficacy of neurorehabilitation. We found that adaptive learning with the hand affects cerebellar-motor cortex connectivity, not only for the trained hand, but also for an untrained leg muscle, an effect likely related to intereffector transfer of learning. Furthermore, we introduce a novel method to measure cerebellar-motor cortex connectivity during movement preparation. With this technique, we show that, outside the context of learning, modulation of cerebellar-motor cortex connectivity is somatotopically specific to the effector being moved.

Keywords: adaptation; cerebellum; connectivity; somatotopy; transcranial magnetic stimulation.

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Figures

Figure 1.
Figure 1.
Experimental design. A, Experiment 1 consisted of five behavioral blocks and three physiological measurements. In Adapt1 and Adapt2, subjects were exposed to a 30° CW cursor rotation; cursor movement was veridical in the remaining blocks. Cerebellar-motor cortex connectivity (CBI) was assessed before Base and after Catch and Adapt2. The numbers in each block represent the number of trials. B, Experiment 2 consisted of 11 behavioral blocks. Adapt1 and Adapt2 had a 30° CW rotation; other blocks were veridical. Red, Right foot movements; blue, right hand movements. There were no physiological measurements for this experiment. C, In Experiment 3, premovement CBI for the FDI was assessed at five different timings (T1–T5) before movement initiation with either the index finger or foot, with T1 at cue onset and T5 being the closest to movement onset. Timings were adjusted to individual RTs. Experiment 4 mirrored the setup of Experiment 3, but premovement CBI was assessed for the TA muscle.
Figure 2.
Figure 2.
Methods. A, Setup for the behavioral task used in all three experiments. Participants viewed the vertical computer monitor for visual feedback about the task and trained with the right hand before switching to the right foot to assess hand-to-foot transfer. For foot movements, the tablet was placed vertically and the foot was propped up. B, Coil placement to measure CBI. This technique requires paired-pulse stimulation in which one TMS coil is placed over M1 (test) and the other over the cerebellum (condition). To determine CBI for the right hand muscle (FDI), the conditioning pulse was delivered over the right cerebellum 5 ms before the test pulse was applied over the left M1 representation of FDI. The same procedure was followed to determine CBI for the right leg muscle (TA), with the test pulse applied over the left M1 representation of TA.
Figure 3.
Figure 3.
Experiment 1 Results. A, End point error (blue line) with SEs (shaded region) during baseline (Base), adaptation (Adapt1 and Adapt2), and catch trials (C). Negative values indicate clockwise deviations caused by the visuomotor perturbation. B, Physiological measure of CBI for both the right FDI (blue) and TA (red). CBI was recorded before any movements (Base) and immediately after catch trials (Catch) and late adaptation (Adapt2). *CBI decreased significantly for both muscle effectors after early perturbation exposure.
Figure 4.
Figure 4.
Experiment 2 Results. A, End point error and SEs for right hand (blue) and right leg (red) movements. Negative values indicate clockwise deviation. B, C, Mean end-point errors in degrees (±SEM) for right leg (red) and right hand (blue) for the baseline and three catch trial epochs. Post hoc analysis revealed significant changes in error for both effectors, indicating hand-to-foot transfer.
Figure 5.
Figure 5.
CBImove. A, B, The x-axis represents CBImove for the right FDI in preparation to moving the hand (A) and foot (B). FDI CBImove measured at five timings (T1–T5) with respect to individual mean response times separately for the hand (blue) and foot (red). *CBI was reduced significantly only in preparation of hand movements. C, CBImove was calculated as the percentage difference from FDI CBI obtained at rest. D, E, The x-axis represents CBImove for the right TA in preparation to moving the foot (D) and hand (E). F, Percentage difference from TA CBI obtained at rest. Positive values indicate disinhibition and negative values increased inhibition. *Only hand movements at 90% RT (T5) modulated CBImove. Data are shown as mean ± SEM.
Figure 6.
Figure 6.
Rest and premovement TS and CS + TS MEP amplitudes. For each participant, we assessed CBI at rest matching the TS MEP amplitudes obtained during CBImove at 90% of RT (TS). CS + TS MEP amplitude (CBI) was only present at rest (green), not when assessed in the context of movement (purple). This indicates that the reduction of CBImove is not due to increased excitability in M1.
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