A New Unifying Account of the Roles of Neuronal Entrainment

Abstract

Rhythms are a fundamental and defining feature of neuronal activity in animals including humans. This rhythmic brain activity interacts in complex ways with rhythms in the internal and external environment through the phenomenon of 'neuronal entrainment', which is attracting increasing attention due to its suggested role in a multitude of sensory and cognitive processes. Some senses, such as touch and vision, sample the environment rhythmically, while others, like audition, are faced with mostly rhythmic inputs. Entrainment couples rhythmic brain activity to external and internal rhythmic events, serving fine-grained routing and modulation of external and internal signals across multiple spatial and temporal hierarchies. This interaction between a brain and its environment can be experimentally investigated and even modified by rhythmic sensory stimuli or invasive and non-invasive neuromodulation techniques. We provide a comprehensive overview of the topic and propose a theoretical framework of how neuronal entrainment dynamically structures information from incoming neuronal, bodily and environmental sources. We discuss the different types of neuronal entrainment, the conceptual advances in the field, and converging evidence for general principles.

Figure 1.

Phase reset vs. entrainment vs. coupled oscillations (see also Box 1). A) Phase reset by a single external event. Phase reset refers to the phase modulation of an oscillating system (brain rhythm) whereby a single event that is external to the oscillating system (e.g. sensory input to cortex) forces the oscillating system into a specific phase at the time point of its occurrence. In the absence of repeated input however (occurrence of one single event), the oscillation slowly reverts to its Eigen-dynamics, as illustrated. B) Entrainment by rhythmic events external to an oscillating system. External rhythmic events result in wavelength modulation and amplitude stabilization of the oscillating system through a series of rhythmic (or quasi-rhythmic) phase-resets (see panel A). The wavelength is modulated to match the period of rhythmic input sequences that sequentially reset the phase of oscillations. C) Phase synchronization of coupled oscillators. This is the result of weak bi-directional coupling of two self-sustained oscillators, which is different from the unidirectional mechanism of entrainment. While theoretically the distinction is clear cut, trying to isolate these mechanisms in the brain might pose significant signal processing challenges.

Figure 2.

Schematic representation of different forms of entrainment during speech. A) Rhythms. Brain rhythms (left panel) and rhythmic forces that can entrain them (right panels), including environmental rhythms, self-produced (bodily) rhythms and rhythmic neuromodulation. Panels B-E) expand on the distinct forms of entrainment with speech (conversation) as an example and underscore the main premise of our review that neuronal entrainment is ubiquitous in the brain and can be driven by very diverse rhythmic forces. During a conversation, environmental sounds produced by a speaker entrain auditory cortex in the listener (B: Entrainment by environmental rhythms), but the associated motor speech production rhythms also lead to neuronal entrainment (C: Entrainment by self-produced rhythms), as do the associated body rhythms, such as respiration (E: Entrainment by body rhythms), while rhythmic neuromodulation can enhance listening performance by entrainment (D: Entrainment by rhythmic neurostimulation). For a detailed description of the scenarios depicted in panels B-E see Box 2.

Figure 3.

Entrainment established phase maps in topographically organized brain regions. A) Sharpening of frequency tuning via entrainment established phase maps in A1. On the left, overlaid frequency tuning curves (thick traces) created from MUA responses (thinner traces to the left of the frequency tuning curves) to attended and ignored stimulus streams from a representative A1 recording site tuned to 4 kHz (the site’s best frequency (BF)). Histograms to the right show the delta phase distribution across single trials at the time of stimulus onset, related to a subset of attended tone streams (shown by arrows), black vertical lines show the mean phase. To quantify the frequency dependent phase opposition related to auditory streams with a frequency matching the BF of the recording site (4 kHz, yellow), vs. non-BF streams, we subtracted the mean phase associated with the BF stream from all mean phases (which is why BF phase (marked by a yellow circle) is 0 in this graph). Next we determined the ratio of the off-BF tone streams that resulted in a mean delta phase (blue circles) at least a half pi different from the BF phase (“outside” a half oscillatory cycle centered on the BF, marked by the blue dotted lines). In this specific case this was 86% (adapted from [168]). B) Scenarios for entrainment established phase maps yielding the same excitability distributions across time and space relative to the focus of attention. Several results in the auditory system hint at the existence of phase maps that “model” the arguably most rudimentary properties of rhythmic auditory streams, frequency and time [31, 61, 168]. This results in a 2-dimensional sharpening of relevant information. We propose that this mechanism can be extended to any topographically mapped brain region (e.g. primary visual or somatosensory cortex, see main text). These phase maps can occur at least in two forms theoretically, both resulting in the same temporal and spatial oscillatory phase established excitability profiles (traces on the bottom and to the right respectively). The first type of phase map (top color map) is one where the region processing attended features is “leading” in phase compared to surrounding ones (peaked waves), resulting in a high excitability phase at attended time points here, and low excitability phases in surrounding regions. The second type of phase map would be established by entraining travelling waves to phases that result in high excitability at the right location and time, which as the traces show, would have the same effect on spatiotemporal excitability as peaked waves. This scenario is intriguing as several studies point at the existence of travelling waves in sensory cortices, yet their role is not yet established (4–6) [–234]. We propose that the reset and entrainment of traveling waves would serve as an ideal mechanism for the rapid deployment of phase-excitability maps across topographically mapped brain regions.