Abstract

Although most activities of daily life require simultaneous coordination of both proximal and distal joints, motor preparation during such movements has not been well studied. Previous results for motor preparation have focused on hand/finger movements. For simple hand/finger movements, results have found that such movements typically evoke activity primarily in the contralateral motor cortices. However, increasing the complexity of the finger movements, such as during a distal sequential finger-pressing task, leads to additional recruitment of ipsilateral resources. It has been suggested that this involvement of the ipsilateral hemisphere is critical for temporal coordination of distal joints. The goal of the current study was to examine whether increasing simultaneous coordination of multiple joints (both proximal and distal) leads to a similar increase in coupling with ipsilateral sensorimotor cortices during motor preparation compared to a simple distal movement such as hand opening. To test this possibility, 12 healthy individuals participated in a high-density EEG experiment in which they performed either hand opening or simultaneous hand opening while lifting at the shoulder on a robotic device. We quantified within- and cross-frequency cortical coupling across the sensorimotor cortex for the two tasks using dynamic causal modeling. Both hand opening and simultaneous hand opening while lifting at the shoulder elicited coupling from secondary motor areas to primary motor cortex within the contralateral hemisphere exclusively in the beta band, as well as from ipsilateral primary motor cortex. However, increasing the task complexity by combining hand opening while lifting at the shoulder also led to an increase in cross-frequency coupling within the ipsilateral hemisphere including theta, beta, and gamma frequencies, as well as a change in the coupling frequency of the interhemispheric coupling between the primary motor and premotor cortices. These findings demonstrate that increasing the demand of joint coordination between proximal and distal joints leads to increases in communication with the ipsilateral hemisphere as previously observed in distal sequential finger tasks.

Highlights

  • The majority of neuroimaging studies in humans focus on simple single-joint tasks due to practical constraints within the MRI scanner

  • We quantified the connectivity within bilateral sensorimotor cortices during motor preparation leading up to movement execution using dynamic causal modeling for induced responses. This allowed us to establish the regions involved in each task, and disentangle the roles of different frequency coupling between tasks. We found that both tasks displayed the expected coupling from contralateral secondary motor areas to contralateral primary motor cortex exclusively restricted to beta band, the simultaneous lifting and opening task elicited increased coupling within the ipsilateral hemisphere towards iM1 that were within and cross-frequencies in theta, beta, and gamma bands

  • We found that participants were reliably able to activate both muscles simultaneously, showing an absolute difference of EMG activation between muscles of 75.7 ± 54.6 ms on average

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Summary

Introduction

The majority of neuroimaging studies in humans focus on simple single-joint tasks due to practical constraints within the MRI scanner. Similar results have been found using EEG during distal-joint movements, where individuals displayed positive coupling from supplementary motor area (SMA) to contralateral motor cortices (Bonstrup et al, 2015; Herz et al, 2012) that matched previous findings showing activation of SMA preceding contralateral M1 Huang et al, 2004. This evidence corroborates results from single-cell recordings in monkeys showing increased prevalence of preparation-related neurons in secondary motor areas compared to M1 Riehle and Requin, 1989 and suggests a cascade-like communication from secondary motor areas to M1 constrained within the contralateral hemisphere

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