Brain rhythms in cognition -- controversies and future directions (2507.15639v1)

Abstract: Brain rhythms seem central to understanding the neurophysiological basis of human cognition. Yet, despite significant advances, key questions remain unresolved. In this comprehensive position paper, we review the current state of the art on oscillatory mechanisms and their cognitive relevance. The paper critically examines physiological underpinnings, from phase-related dynamics like cyclic excitability, to amplitude-based phenomena, such as gating by inhibition, and their interactions, such as phase-amplitude coupling, as well as frequency dynamics, like sampling mechanisms. We also critically evaluate future research directions, including travelling waves and brain-body interactions. We then provide an in-depth analysis of the role of brain rhythms across cognitive domains, including perception, attention, memory, and communication, emphasising ongoing debates and open questions in each area. By summarising current theories and highlighting gaps, this position paper offers a roadmap for future research, aimed at facilitating a unified framework of rhythmic brain function underlying cognition.

• The paper reviews oscillatory mechanisms such as phase, amplitude, and cross-frequency coupling as key drivers in cognitive processes.
• The paper illustrates methodological advancements with data-driven EEG/MEG approaches that reveal individual-specific frequency variations impacting cognition.
• The paper discusses integrating neural oscillations with bodily rhythms, outlining controversies and proposing directions for future research.

Brain Rhythms and Cognition: A Comprehensive Review

This paper (2507.15639) offers an extensive review of the current understanding, controversies, and future directions in the paper of brain rhythms and their relationship to cognition. It synthesizes findings across multiple cognitive domains, emphasizing the importance of oscillatory mechanisms and highlighting gaps in the existing literature.

Putative Oscillatory Mechanisms

The paper categorizes oscillatory mechanisms based on their phase, amplitude (or power), and frequency, each linked to distinct physiological functions. At the neuronal level, oscillations reflect fluctuations in neuronal excitability, regulated by interactions between excitatory pyramidal neurons and inhibitory interneurons. The authors note human brain rhythms are conventionally separated into canonical frequency bands such as delta, theta, alpha, beta, and gamma. They emphasize the limitations of early EEG recordings, noting recent data-driven approaches reveal that frequency bands can vary considerably between individuals, brain anatomy, and tasks.

Mechanisms of Oscillatory Phase

The paper discusses how the instantaneous phase of an oscillation reflects the momentary state of an oscillating system within its cycle. Synchronized oscillators, where peaks and troughs align, are examined for their mechanistic links to cognitive function.

• Excitation-Inhibition Cycle: The paper reviews early evidence suggesting that the phase of cortical oscillations reflects the cortex's momentary excitability, influencing sensitivity to sensory stimulation. High-excitability phases correlate with higher neuronal firing rates, creating a temporal scaffolding for information processing across frequency bands. The paper notes measures of phase opposition can be used to distinguish high- and low-excitability phases.
• Synchronization Between Neuronal Populations: Neuronal oscillations are invariably associated with neuronal phase synchronization between distinct oscillating populations. The communication-through-coherence (CTC) hypothesis suggests that synchronized firing allows flexible establishment of stable communication channels across the brain. The authors challenge the functional role of rhythmic activity in communication between neuronal populations by introducing the "Synaptic-Source-Mixing" (SSM) model.
• Sensory Entrainment: Sensory entrainment involves rhythm-generating neuronal populations synchronizing to periodicities in external sensory input. The authors note challenges in discerning whether spectral peaks reflect the tracking of periodic input dynamics or the involvement of entrained neural oscillators. The paper states direct evidence for sensory entrainment is sparse.

Mechanisms of Oscillatory Power

The paper analyzes amplitude or power as measures of the strength of oscillations and introduces the neural processes hypothesized to underlie neuronal power dynamics.

• Macroscopic Measures and Excitation-Inhibition Balance: Higher amplitude reflects more widespread synchronization within a neural population. The paper links amplitude/power levels of low frequencies to a state of inhibition, particularly in the alpha band. It also investigates how excitation/inhibition (E/I) balance affects the power spectrum and discusses approximations developed to infer underlying E/I balance from EEG/MEG data.
• Gating by Inhibition: The paper links alpha amplitude to the gating of information of neural signals. It notes gating could occur at the network or local level, influencing the transfer of information between nodes, or up- or down-regulating local excitability. It also considers the level at which alpha amplitude may gate processing of information.
• Predictive Processing: The paper relates neural oscillations to predictive processing, where lower-frequency activity tends to carry predictions in feedback directions, while higher-frequency activity is associated with prediction errors carried forward. Recent work suggests this mapping may be overly simplistic.

Cross-Frequency Coupling Mechanisms

Cross-frequency coupling (CFC) is explored as a mechanism that integrates and coordinates different elementary operations involved in cognitive function. Established forms of CFC, such as phase-amplitude, phase-phase, and amplitude-amplitude coupling, are examined, although others have also been proposed. The authors note the exact relationship between different forms of CFC is still debated.

Traveling Waves

The paper considers the spatial organization of brain oscillations across the cortex, including how they propagate as traveling waves. Mesoscopic oscillatory traveling waves are defined as smooth phase shifts between recording locations within a single brain area, while macroscopic waves can span the whole cortex. The paper raises the question of whether spatial propagation is an intrinsic feature of neural oscillations.

Resting-State Rhythmic Activity

The brain's activity at rest exhibits highly structured spatiotemporal patterns. The paper notes the most prominent resting-state activity is likely the parieto-occipital alpha rhythm, with other large-scale rhythmic activity across the cortex, such as frontal theta and temporal gamma, also described. The authors emphasize both local rhythmic activity and oscillatory networks at rest show large inter-individual variability.

Interactions with Other Bodily Rhythms

The link between neural oscillations and human cognition is expanded to include modulatory influences from body physiology such as respiration, cardiac activity, pupil dynamics, and gastrointestinal signals.

• Respiration: The paper describes how nasal respiration modulates neural oscillations across a wide cortico-subcortical network. It notes the modulatory behavioral effects of respiration have been shown in perceptual, motor, and cognitive tasks.
• Pupil-Linked Arousal: Recent studies combining pupillometry and MEG/EEG provide evidence that neuromodulatory arousal has distinct effects on different cortical regions, and rhythmic activity in different frequency bands in the human brain. The pupil also engages in its own resting rhythm, the Hippus, with a frequency of around 0.2 Hz.
• Cardiac Rhythms: Heart-brain interactions are modulated by sympathovagal activity and have a direct influence on the insula, amygdala, hippocampus, and cingulate cortices. Cardiac fluctuations are thought to instantiate alternating time-windows of high- and low-excitability.
• Gastric Rhythms: A recent MEG paper showed that the amplitude of alpha rhythms in the parieto-occipital cortex and the right anterior insula is modulated by the phase of the gastric rhythms.
• Circadian Rhythms: The circadian cycle modulates neural activity, humor, and behavior via the HPA axis, thus regulating glucocorticoid hormones. The paper notes it will be an important step forward to understand the coupling of oscillations at vastly different time scales.

Oscillatory Mechanisms and Their Role in Cognition

The paper connects oscillatory mechanisms with cognitive functions, highlighting open questions and debates within specific cognitive domains.

Perception and Attention

• Visual Perception and Attention: Brain rhythms, especially alpha, seem to index the momentary excitability of our visual cortex to incoming stimulation. Strong parieto-occipital alpha oscillations impede detection of visual targets. The accuracy of detecting peripheral targets varies with a period that falls into the theta frequency range.
• Auditory Perception and Attention: The auditory cortical system exhibits distinctive rhythmic activity during rest and active listening. However, oscillatory mechanisms in auditory perception do not seem to be a mere copy of those found in vision. The paper notes it is often unclear how oscillatory phenomena are relevant to attentional selection behaviorally.
• Multisensory Perception and Attention: Processing sensory input provided by multiple channels requires weighing, integrating and segregating auditory, visual, tactile, and other input. A question that persists is how multisensory percepts form and are represented neurophysiologically.

Memory

• Working Memory: Alpha power generally increases during memory maintenance, and further increases with memory load. Multi-item working memory relies on the ability to link related features constituting a perceptual object. Oscillations play a critical role in solving these problems.
• Long-Term Memory: Theta and gamma oscillations in the hippocampus have been suggested to coordinate spike timing for synaptic weight changes, thus contributing to memory formation. The paper notes while similar evidence has been found in the human brain, there are some discrepancies.

Communication

• Speech and Language Processing: Speech recognition poses a challenge for the brain, requiring the identification of linguistic units from a continuous signal. Theoretical proposals suggest brain rhythms in the auditory cortex entrain to quasi-rhythmic occurrences of linguistic units, allowing for speech segmentation.
• Speech Production and Motor Involvement in Language Processing: Speech production requires the precise temporal coordination of auditory, linguistic, motor, and predictive processes. The anticipation of movement typically involves suppression of oscillatory power in the beta-range.
• Music and Rhythm Processing: Low-frequency neural dynamics track the amplitude fluctuations in the acoustic envelope of music. Synchrony to the note rate is thought to be related to temporal prediction and attention.

Conclusion

The review emphasizes the importance of brain rhythms as a pivotal link tying cognitive function to neuronal processes. However, it raises challenges that the field will need to overcome, particularly whether brain rhythms have the causal role we typically assume.