Review article
Prominence of delta oscillatory rhythms in the motor cortex and their relevance for auditory and speech perception

https://doi.org/10.1016/j.neubiorev.2019.09.012Get rights and content

Highlights

  • Delta (0.5–4 Hz) oscillations are endogenous rhythms of the motor system and can be generated independently from motor beta oscillations.

  • Motor delta oscillations encode neural motor trajectories and are visible in the dynamics of most basic motor acts.

  • Motor delta oscillations encode sensory temporal contextual information.

  • Motor delta oscillations shape sensory processes by imposing temporal constraints on the sampling of sensory information.

  • Motor delta oscillations optimize the parsing, encoding and processing of slow linguistic information.

Abstract

In the motor cortex, beta oscillations (∼12–30 Hz) are generally considered a principal rhythm contributing to movement planning and execution. Beta oscillations cohabit and dynamically interact with slow delta oscillations (0.5–4 Hz), but the role of delta oscillations and the subordinate relationship between these rhythms in the perception-action loop remains unclear. Here, we review evidence that motor delta oscillations shape the dynamics of motor behaviors and sensorimotor processes, in particular during auditory perception. We describe the functional coupling between delta and beta oscillations in the motor cortex during spontaneous and planned motor acts. In an active sensing framework, perception is strongly shaped by motor activity, in particular in the delta band, which imposes temporal constraints on the sampling of sensory information. By encoding temporal contextual information, delta oscillations modulate auditory processing and impact behavioral outcomes. Finally, we consider the contribution of motor delta oscillations in the perceptual analysis of speech signals, providing a contextual temporal frame to optimize the parsing and processing of slow linguistic information.

Section snippets

Intrinsic oscillatory activity in the motor cortex

Cortical rhythms reflect synchronous, periodic shifting of neuronal ensembles between high and low excitability states, that coordinates neural communication (Schroeder et al., 2008; Schroeder and Lakatos, 2009; Buzsáki and Draguhn, 2004; Wang, 2010). In the motor cortex, the vast majority of existing data point to beta oscillations (∼12-30 Hz; frequency borders based on Buzsaki, 2006, p.112) as a predominant and specific rhythm during rest and to coordinate information transfer in action

Rhythmic sampling of perceptual information

In an active sensing framework, perception is shaped by motor dynamics (Morillon et al., 2015). Indeed, our sensory organs are not passive receptacles for stimulation but are part of an action-perception closed-loop system (Kleinfeld et al., 2006; Schroeder et al., 2010; Ahissar and Assa, 2016; Rajkai et al., 2008; Barczak et al., 2019). Consequently, motor acts and associated oscillatory dynamics temporally structure the activity of sensory cortices, and, as a consequence, the processing of

Temporal predictions in auditory attention

When sensory signals hold a recurring temporal structure, they enable a proactive and temporally selective preparation for anticipated relevant events (Nobre and van Ede, 2018; Rimmele et al., 2018). Acoustic signals such as speech and music exhibit reliable temporal regularities that can be used to generate temporal predictions (Ding et al., 2017). Behavioral experiments demonstrate that anticipating the temporal occurrence of an upcoming event optimizes its processing by improving the quality

Motor contributions to speech perception

Human speech is in essence structured in the temporal dimension, with nested dynamics organized according to a hierarchy of linguistic timescales (phoneme, syllable, word, phrase; (Giraud and Poeppel, 2012; Ding et al., 2016; Keitel et al., 2018; Schroeder et al., 2008). Although speech is not strictly periodic, its regularities are visible as peaks in the power and modulation spectrum of the speech envelope (Ding et al., 2017; Keitel et al., 2018). Remarkably, these acoustic dynamics are

Conclusions

The studies reviewed above provide evidence that delta oscillations are intrinsic in the motor cortex and critically shape both overt motor behaviors and covert motor-related modulation of sensory neural processes. They reflect a behavioral time-constant that is directly interpretable in a cognitive framework. This delta motor activity often seems to be intrinsically linked to beta oscillations through cross-frequency coupling, but the relationship between delta and beta rhythms is dynamic and

Acknowledgments

B.M was supported by grants from the ANR (Agence Nationale pour la Recherche, France), the ILCB and BLRI, respectively, ANR-16-CONV-0002 (ILCB), ANR-11-LABX-0036 (BLRI) and the Excellence Initiative of Aix-Marseille University (A*MIDEX). C.E.S. supported by R01 MH111439 and P50 MH109429.

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