Abstract
Modulation of gamma oscillations recorded from the human motor cortex and basal ganglia appears to play a key role in movement execution. However, there are still major questions to be answered about the specific role of cortical gamma activity in both the planning and execution of movement features such as the scaling of peak velocity and movement time. In this study, we characterized movement-related gamma oscillatory dynamics and its relationship with kinematic parameters based on 256-channels EEG recordings in 64 healthy subjects while performing fast and uncorrected reaching movements to targets located at three distances. In keeping with previous studies, we found that movement-related gamma synchronization occurred during movement execution. As a new finding, we showed that gamma synchronization occurred also before movement onset, with planning and execution phases involving different gamma peak frequencies and topographies. Importantly, the amplitude of gamma synchronization in both planning and execution increased with target distance and predicted peak velocity and movement time. Additional analysis of phase coherence revealed a gamma-coordinated long-range network involving occipital, frontal and central regions during movement execution that was positively related to kinematic features. This is the first evidence in humans supporting the notion that gamma synchronization amplitude and phase coherence pattern can reliably predict peak velocity amplitude and movement time. Therefore, these findings suggest that cortical gamma oscillations have a crucial role for the selection, implementation and control of the appropriate kinematic parameters of goal-directed reaching movements.
Highlights
Voluntary movements are accompanied by modulation of oscillatory activity of both the beta (13.5–25 Hz) and gamma frequency ranges (25.5–90 Hz) that have been consistently observed with EEG, MEG and ECoG over the sensorimotor cortex and with electrode recordings in basal ganglia structures (Kilavik et al, 2013; Nowak et al, 2018).Gamma Modulation and Kinematic FeaturesMovement-related beta oscillatory event-related desynchronization (ERD) and synchronization (ERS) have been characterized to a great extent in both healthy and clinical populations (Kilavik et al, 2013; Little and Brown, 2014; Cao and Hu, 2016; Barone and Rossiter, 2021)
We have demonstrated that the movement-related beta ERD-ERS dynamics does not depend on target distance, movement length or peak velocity (Tatti et al, 2019)
We parametrically explored the relationship between movement distance and peak velocity on movement-related gamma ERS in a large group of healthy subjects
Summary
Voluntary movements are accompanied by modulation of oscillatory activity of both the beta (13.5–25 Hz) and gamma frequency ranges (25.5–90 Hz) that have been consistently observed with EEG, MEG and ECoG over the sensorimotor cortex and with electrode recordings in basal ganglia structures (Kilavik et al, 2013; Nowak et al, 2018).Gamma Modulation and Kinematic FeaturesMovement-related beta oscillatory event-related desynchronization (ERD) and synchronization (ERS) have been characterized to a great extent in both healthy and clinical populations (Kilavik et al, 2013; Little and Brown, 2014; Cao and Hu, 2016; Barone and Rossiter, 2021). The results of some ECoG studies of gamma ERS in the human primary somatosensory cortex (Miller et al, 2007; Avanzini et al, 2016; Ryun et al, 2017) have suggested an association between gamma oscillations and the proprioceptive feedback ensuing movement and sensorimotor input This hypothesis has been challenged by reports showing that passive movements do not elicit gamma synchronization (Muthukumaraswamy, 2010; Brücke et al, 2012) and that mirror illusion in absence of proprioceptive feedback prompts movement-related gamma ERS (Butorina et al, 2014). Links between gamma ERS amplitude and the amount of force generated have been described by EcoG studies of the motor cortex of epileptic patients (Flint et al, 2014; Jiang et al, 2020), by recordings in the subthalamic nucleus of patients with Parkinson’s disease (Tan et al, 2013a, 2016) and by a MEG study over the contralateral sensorimotor region of eight normal subjects (Muthukumaraswamy, 2010). Some relationships between gamma power and movement amplitude and velocity have been found with recordings in the globus pallidus of dystonic patients (Brücke et al, 2012) and in the subthalamic nucleus of patients with Parkinson’s disease (Lofredi et al, 2018), respectively
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