Modulation of Gamma and Theta Spectral Amplitude and Phase Synchronization Is Associated with the Development of Visuo-Motor Learning

Abstract

The formation of new motor memories, which is fundamental for efficient performance during adaptation to a visuo-motor rotation, occurs when accurate planning is achieved mostly with feedforward mechanisms. The dynamics of brain activity underlying the switch from feedback to feedforward control is still matter of debate. Based upon the results of studies in declarative learning, it is likely that phase synchronization of low and high frequencies as well as their temporal modulation in power amplitude underlie the formation of new motor memories during visuo-motor adaptation. High density-EEG (256 electrodes) was recorded in 17 normal human subjects during adaptation to a visuo-motor rotation of 60° in four incremental steps of 15°. We found that initial learning is associated with enhancement of gamma power in a right parietal region during movement execution as well as gamma/theta phase coherence during movement planning. Late stages of learning are instead accompanied by an increase of theta power over that same right parietal region during movement planning, which is correlated with the degree of learning and retention. Altogether, these results suggest that the formation of new motor memories and thus, the switch from feedback to feedforward control, is associated with the modulation of gamma and theta spectral activities, with respect to their amplitude and phase, during movement planning and execution. Specifically, we propose that gamma/theta phase coupling plays a pivotal role in the integration of a new representation into motor memories.

Oscillatory entrainment of the motor cortical network during motor imagery is modulated by the feedback modality

“…Oscillations in the θ-band are linked to working memory processes (Brookes et al, 2011;Osipova et al, 2006), long-term memory formation and retrieval of motor schemata (Perfetti et al, 2011). The inter-regional functional coupling of brain structures in the θ-band is also necessary for the emergence of visuospatial working memory during motor planning, motor skill learning and target selection during movements (Kaplan et al, 2012;Rawle et al, 2012;Sauseng et al, 2010).…”

Brain representations for acquiring and recalling visual–motor adaptations

“…Prior work has already implicated parietal structures in sensory-motor memory formation (Della-Maggiore et al 2004; Inoue et al 1997; Mutha et al 2011; Perfetti et al, 2011). However, there remains some controversy whether the left or the right parietal cortex has more importance for learning.…”

Redistribution of neural phase coherence reflects establishment of feedforward map in speech motor adaptation

“…For each trial epoch, an overlapping 800-ms time-window that was slid by 10 ms in each time step was used, and, for the frequency bands, a 3-Hz frequency window with 1-Hz step was used. The EEG signal of the gamma band (upper frequency band) was first band-pass filtered before obtaining power time series by squaring the amplitude of its Hilbert transformation (Cohen 2008;Perfetti et al 2011). The power time series of the upper frequency was then used to compute its instantaneous phase.…”

“…In recent years, the role of neuronal oscillations and crossfrequency phase coupling, particularly in the theta (3)(4)(5)(6)(7)(8) and gamma bands, has been demonstrated in a variety of cognitive and sensorimotor tasks in humans involving working memory (Herrmann et al 2010), spatial navigation (Burke et al 2013), perceptual grouping (Gray et al 1989), visuomotor integration (Roelfsema et al 1997) and adaptation (Perfetti et al 2011). Similar phase coupling has been shown for working memory tasks in monkeys (Lee et al 2005) and for associative learning in rats (Tort et al 2009).…”