The Strength of Alpha–Beta Oscillatory Coupling Predicts Motor Timing Precision

Abstract

Precise timing makes the difference between harmony and cacophony, but how the brain achieves precision during timing is unknown. In this study, human participants (7 females, 5 males) generated a time interval while being recorded with magnetoencephalography. Building on the proposal that the coupling of neural oscillations provides a temporal code for information processing in the brain, we tested whether the strength of oscillatory coupling was sensitive to self-generated temporal precision. On a per individual basis, we show the presence of alpha-beta phase-amplitude coupling whose strength was associated with the temporal precision of self-generated time intervals, not with their absolute duration. Our results provide evidence that active oscillatory coupling engages ␣ oscillations in maintaining the precision of an endogenous temporal motor goal encoded in ␤ power; the when of self-timed actions. We propose that oscillatory coupling indexes the variance of neuronal computations, which translates into the precision of an individual's behavioral performance.Which neural mechanisms enable precise volitional timing in the brain is unknown, yet accurate and precise timing is essential in every realm of life. In this study, we build on the hypothesis that neural oscillations, and their coupling across time scales, are essential for the coding and for the transmission of information in the brain. We show the presence of alpha-beta phaseamplitude coupling (␣-␤ PAC) whose strength was associated with the temporal precision of self-generated time intervals, not with their absolute duration. ␣-␤ PAC indexes the temporal precision with which information is represented in an individual's brain. Our results link large-scale neuronal variability on the one hand, and individuals' timing precision, on the other.

Common and distinct roles of frontal midline theta and occipital alpha oscillations in coding temporal intervals and spatial distances

“…This perceptual resolution account is also suggested by Samaha and Postle (2015) showing that occipital alpha frequency reflects the "refresh rate" of visual perception and occipital alpha represents the perceptual unit of temporal processing (Cecere et al, 2015). Consistent with this view, we predict that occipital alpha frequency should affect not only the encoding but also the retrieval and reproduction of temporal intervals, given that tACS-induced shifts in resting alpha frequency lead to shifts in subjective time experiences (Mioni et al, 2020), alpha-beta phase amplitude coupling correlates with time reproduction precision (Grabot et al, 2019), and that alpha frequency is central to the strengths of alpha-beta coupling. Future studies could investigate how interval reproduction performance is associated with alpha frequency modulation in healthy humans, as well as in the pre-clinical Alzheimer populations which show irregularities in parietal alpha oscillations (Montez et al, 2009).…”

“…Second, we found that oscillatory codes for temporal judgments were influenced by past trials while such codes for spatial judgments were not. Consistent with the idea of separable representations for space and time, spatial and temporal discounting are behaviorally distinctive from each other (Robinson, Michaelis, Thompson, & Wiener, 2019), estimating spatial distance can be subject to large errors (Zhao, 2018) while estimating suprasecond intervals can be performed with relatively high accuracy (Grabot et al, 2019), and spatial and temporal estimation errors distort in opposing manners (Brunec, Javadi, Zisch, & Spiers, 2017). The dissociation between space and time are also supported at the level of oscillatory signatures.…”

“…Some studies have looked at patterns of cortical low-frequency power when participants remember supra-second intervals. For example, the alpha-beta coupling strengths predict the precision of time reproduction (Grabot et al, 2019), and theta power in striatum and sensorimotor cortex discriminate rats' responses to THETA, ALPHA AND SPACE-TIME CODING 4 temporal interval comparisons (Gu, Kukreja, & Meck, 2018). Abundant evidence from single-unit recordings also suggests medial temporal lobe (MTL) structures form internally-generated assembly whose firing activities track time passage on scale of seconds (Itskov, Curto, Pastalkova, & Buzsáki, 2011;MacDonald, Lepage, Eden, & Eichenbaum, 2011;Pastalkova, Itskov, Amarasingham, & Buzsáki, 2008;Wang, Romani, Lustig, Leonardo, & Pastalkova, 2015).…”

Movement Improves the Quality of Temporal Perception and Decision-Making

“…Likewise, auditory frequency discrimination performance is impaired when subjects receive stimulation to the somatosensory cortex, but only when they are required to simultaneously attend to touch (Convento et al, 2018). Similarly, recent research has begun to demonstrate that time perception is highly linked to the amplitude and phase of beta (13–30 Hz) oscillations (Arnal et al, 2015; Kulashekhar et al, 2016; Wiener and Kanai, 2016; Morillon and Baillet, 2017; Grabot et al, 2019). That beta oscillations are also highly implicated in movement is likely no coincidence; movement and timing may be intrinsically linked.…”

Interactions Between Motor Thalamic Field Potentials and Single-Unit Spiking Are Correlated With Behavior in Rats

“…Oscillations of different frequencies are commonly coupled to each other, both within and between brain regions (Lakatos et al, 2005 ; Canolty et al, 2007 ). For example, delta phase is correlated with beta oscillation amplitude (Saleh et al, 2010 ; López-Azcárate et al, 2013 ; Arnal et al, 2015 ; Hamel-Thibault et al, 2018 ; Grabot et al, 2019 ), and beta phase is correlated with the amplitude of higher frequency oscillations (de Hemptinne et al, 2013 ; Meidahl et al, 2019 ). These complex correlations provide rich information regarding neural dynamics but make it difficult to distinguish cause from effect.…”