Rhythms in cognition: The evidence revisited

European Journal of Neuroscience, Journal Year: 2022, Volume and Issue: 55(11-12), P. 2991 - 3009

Published: June 1, 2022

Brain activity abounds with rhythmic patterns (Capilla et al., 2021; Groppe 2013; Keitel & Gross, 2016) that reflect ongoing fluctuations of neuronal excitability (Adrian Matthews, 1934; Bishop, 1932). These rhythms can be described as oscillations cycle through phases at specific frequencies and a certain strength or amplitude (Figure 1). Attempts to account for the functional relevance have gone from associating cognitive function X Y more comprehensive understanding role brain in human everyday experience behaviour (Buzsáki Draguhn, 2004; Fries, 2015; Lakatos 2019; Wang, 2010). accounts support simple, yet fundamental idea: Cognitive functions themselves may intrinsically rhythmic. "The scanning apparatus should intrinsic period operation which identifiable performance brain. [...] In fact, it has order frequency appropriate alpha rhythm brain, shown electroencephalograms. We suspect this is associated form perception, partakes nature sweep rhythm, like process television apparatus." Theories derived these early ideas been reiterated over past 90 years. During time, research focussed on variations framework claiming processes depend offered wealth empirical evidence (Schroeder 2010; VanRullen, 2016; VanRullen Koch, 2003). Rhythmic sampling, implemented rhythms, proposed underlies not only perception but also attention (VanRullen 2007), memory (Staresina 2015), language (Giraud Poeppel, 2012). Linking cognition sampling particularly attractive because allows using global mechanistic principles bridge two different levels explanation: normal function, involves activity, experiences. addition, leaves open possibility actively intervening external stimulation either advance theory, example, close causal (see section 'Can we manipulate take control cognition?'), develop applications clinical interventions, such rehabilitation, brain-computer interfaces. The field, however, immune controversy. available does unequivocally assumed visual processing (Benwell 2017; Chaumon Busch, 2014; Fekete 2018; O'Hare, 1954; Ruzzoli van Diepen Van Walsh, 1952), various theoretical inconsistencies highlighted (Fekete White, 2018). For instance, exact implicated often differ between studies task and/or stimulus characteristics (Chen 2020; Ho Merholz 2022; Ronconi see table 2019), difficult reconcile any simple model fixed, discrete temporal 'frames' (White, Additionally, effect sizes showing periodicity behavioural neural measures tend small, hence line clear, all-or-nothing frame boundaries (Milton Pleydell-Pearce, 2018) utility real-life (Vigué-Guix 2020). Furthermore, literature suffers lack direct replications, pre-registered studies, data, code sharing (Garrett-Ruffin Niso Pavlov 2021), well low statistical power (Button 2013). Finally, publication bias favour statistically significant results distorted undermined reliability published (Szucs Ioannidis, 2017). Despite extensive research, existence remain intensely debated, idea continues attract vast interest. Special Issue, called methodologically principled irrespective their outcome, would contribute clarifying if, under conditions, observed. addition 26 original articles (including conceptual replications), received reviews, methodological advances, position papers. Following our aim re-visit cognition, evaluated primary outcomes 23 tested hypothesis directly. A split picture emerged 11 reporting supportive 12 others null inconclusive findings Figure 2). Within context, here review 36 publications Issue an emphasis how each contribution informs questions controversies wider cognition. doing so, cluster contributions around prevalent topics – Does operate rhythmically? And if processes? majority come influence outcomes. Below, summarise previous lines discuss relevant Issue. Numerous demonstrated by probing time intervals relative reference event. Provided are distributed across wide-enough range sampled densely within range, resulting course submitted spectral analysis rhythmicity. This approach new (e.g., Latour, 1967; Purushothaman 2000) become increasingly popular last decade Dugué Fiebelkorn Landau 2012; Senoussi 2019). refer reader Kienitz al. (2021) overview experimental paradigms employed study during attentive vision both non-human primates. behaviour, debate surrounds potential dissociations frequencies. Michel addressed topic information up down theta (4–7 Hz) (8–12 rhythms. participants performed orientation judgement after non-informative cue (50% validity) indicated target location. observed precision oscillated invalidly cued targets, whilst guess rate validly targets. suggest distinct roles potentially subserving attentional fluctuations. However, authors suggested environmental likely drives spatial resolution, rather than strict succession perceptual snapshots blind gaps 'up' 'down' respectively. possible frequencies, degree fixed depends demands participant state remains unclear. regard, Balestrieri (2021, issue) showed interplay working memory. Rhythms detection were maintenance simultaneous task. Interestingly, was modulated load, oscillating ~7.5 Hz versus 5 high respectively, suggesting might depending allocation limited resources another Morrow Samaha whether occurs alpha-band (Chakravarthi Sokoliuk 2016), capitalising motion-related illusions: flash-lag Fröhlich effect. Indeed, according recently (K. A. Schneider, 2018), supported series 'perceptual moments', duration individual differences illusions. hypothesised effects driven endogenous peak participants, then magnitude illusion correlated individuals. successfully induced illusions all found no correlation Bayesian favoured single underlying oscillatory mechanism could Plöchl examined auditory modality. Their included visual, auditory, bimodal conditions task, closely replicated seminal Fries (2012). Specifically, they capitalised reset (in modality) automatically drive one (left vs. right) streams events uncued locations. fluctuated counter phase attended locations, confirming supramodal processing. modality entirely earlier finding where alpha-range (9 response decision making (Ho combined dichotic oddball paradigm test violating sensory expectations made novel observation stimuli played non-anticipated ear induce subsequent theta-range (7.6 accuracy. update representations following violations expectations. concluded that, although rhythmicity corroborated (growing) number special considerations analytical necessary Brookshire, 2021). need chosen, require large trials participants. On note, der Werf unable replicate (Fiebelkorn Helfrich modified Egly-Driver (Egly 1994) detecting appear end (i.e., location) other space-based, non-cued bar, equidistant bar (object-based, location). No pattern accuracy locations level predictive validity, though exploratory did reveal ~7–8 when cues moderately informative. commentary al.'s study, proposes despite being comparable (Helfrich per condition replication too reliably detect further suggests purely data limiting combining simultaneously recorded electrophysiology (but ten Oever 2022, issue, Fiebelkorn's commentary). Magneto- electroencephalography (M/EEG) allow investigating activity. They enable analyses performance, detection, parameters (phase amplitude) presentation. Most M/EEG revolve question pre-stimulus affect attempting specific, previously untested conditions. EEG presented detected targets rhythmically counter-phase predicted modalities. Benwell challenging letter identification measure subjective awareness trial. confirmed reports (also By contrast, had accuracy, again replicating 1952). Similarly, Michail discrimination corresponding phase. unique aspect experiment long 2.5 s. Accordingly, speculate less lasting several cycles. Sheldon Mathewson set out post-stimulus likelihood guessing. reproduced precisely analysed error distribution models yield separate estimates Conceptually, similar who 'Rhythmicity behaviour'). (Mathewson 2009; Fakche 2022), performance. Instead, 2–7 activities Zazio issue), turn, clear behaviour. resembled (Busch 2009), reported Using MEG source analysis, stimulus-evoked inversely related occipito-temporal areas, whereas localised occipital prefrontal areas. Whilst assessed analysing Es (2020, used vector machine decode (counter/clockwise) signal. classification along theta/alpha frontal eye field parietal cortex contralateral grating stimulus. reflected (reaction times), leaving unknown. Gaillard Ben Hamed neurophysiological argue seems continuously regions alternates periodically center periphery parieto-frontal networks. two-stage positing combination continuous interact conscious percepts (Herzog Vigué-Guix attempted demonstrate interesting features stand section. First, aimed Callaway Yeager (1960), papers looking into idea. closed-loop analyse real-time (bright LED flashes) selectively rhythm. Second, kept eyes closed throughout experiment, amplified facilitated extracting its comparably small sample demonstrating level. reliable estimation parameter managed present accordingly, onset times participant. putative sizable enough practical relevance, signal interface applications. Along phase, recent investigated instantaneous within- between-participant integration temporally proximal (Samaha Postle, 2015) multisensory (audiovisual) (Cecere Keil Senkowski, 2017), theory cycles (VanRullen, 2016). London (2022, extend audiovisual supra-threshold stimuli. occipito-parietal electrodes increased sensitivity, found. results, those (Buergers Noppeney, cast doubt notion determining factor sensitivity perception. provided reviewed thus far provide answer way Behavioural issue frequently perhaps surprising contrasts suggestion (Fiebelkorn, 2021, given represents measurement question. tasks appears quite robust, (see, e.g., D. Schneider (Zazio Therefore, markedly weaker compared effects. aligns Benwell, Keitel, Notably, even subset considered attempts (Plöchl Der least very designs (van mixed. Replication extension key will critical development (Pavlov valuable examples. It crucial methodologies optimised 2022). flaws (such power), important validated replications. ideally trial numbers) terms overall size. collaborative run labs (Open Science Collaboration, 2015). Another future step derive hypotheses existing theories about tasks, states (and not). 1932) predicts is, excitability. arguably case short durations contrast feature longer (Michail Mathewson, issue). challenge define benchmark 'just works', stimuli, trusted fields neuroscience developed conventional eliciting interest, capture (Theeuwes, 1992), cueing (Carrasco, 2011), markers (Ngiam Establishing standard vantage point chart determine affects Manipulating periodic tool sampling. As Quigley reports, dates back Adrian Matthews (1934) Walter (1954), light light-induced responses synchronisation inputs since termed 'entrainment'. entrainment remained pervasive drew strengths major routes: explanatory functions, versatility technique experimenters and, later on, interventionists. Regarding power, Dynamic Attending Theory, posits internal oscillators rhythms) synchronise (Jones Boltz, 1989; Henry Herrmann, 2014). Once established, synchronised cycling optimal cortical coincide upcoming facilitates Lakatos, 2009). widely promoted general interactions input (Lakatos Tavano emblematic crucially underlie ability tune segment understand speech Rimmele Hauswald 2020, From perspective experimenters, versatile method directly manipulating Next stimulation, magnetic electrical non-invasive (NIBS) (Thut, Schyns, 2011). prospect influencing inspired interventions pathological please Tichko (2020) gamma-frequency (40 attempt counteract pathophysiologies linked Alzheimer's disease (Iaccarino strong integrating music-based currently therapy. enthusiastically overall, unclear, implementing applies circumscribed situations. One significance benefits beyond regularities input. implements selective (Calderone 2013), facilitate behaviourally providing periods Barne predictably recurring (here: tone frequency) lead higher predictable features, embedded regular sequences. interleaved instructed compare them probe brief retention interval. Although find benefit non-rhythmic de Graaf Duecker, W. M. Lin, Oetringer, Rassili Ordin, Sun nor pre-probe templates period, cortices intermittent pre-activation anticipation anticipatory anti-phasic activation supports puts maximally excitable (potential) delivery. Moreover, self-sustain ceases. Lin three experiments versions pitch total 181 occurring discriminated faster accurately out-of-phase. first experiments, low-frequency 1–3 Hz. paradigm, Hickok (2015) in-phase easily, entrainment. findings. After amplitude-modulated noise, responded tones constant noise pre-target noise. some periodicities consistently Saberi Hickok, Ordin presenting sequence (linguistic) syllables (non-linguistic) natural sounds similarly affected intermediately sound. neither type exceeded irregular Further hinted reactio

Language: Английский

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Representation of vocalizations in the frontal auditory field and the dorsal auditory cortex of bats

Annals of the New York Academy of Sciences, Journal Year: 2025, Volume and Issue: unknown

Published: April 8, 2025

Abstract In bats, which express a complex vocal repertoire and are considered learners, the frontal auditory field (FAF) is supposedly placed in cortico‐striatal network for vocal–motor control. The FAF receives input from cortex (AC) other nuclei via multiple pathways. However, not much known about transition of information on vocalizations AC to FAF. bat consists different subfields, among dorsal fields (dAC) characterized by precise coding temporal envelope vocalizations. dAC should, therefore, be major source feedback self‐produced or perceived Our study aimed investigate specificity encoding types neurons. Using extracellular recordings anesthetized Phyllostomus discolor , we describe basic response properties both cortical areas compare responses prerecorded behaviorally relevant call categories single calls was higher than neurons, terms firing patterns strength. These findings highlight importance neural control communication bats.

Language: Английский

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Oscillatory Waveform Shape and Temporal Spike Correlations Differ across Bat Frontal and Auditory Cortex

Journal of Neuroscience, Journal Year: 2024, Volume and Issue: 44(10), P. e1236232023 - e1236232023

Published: Jan. 23, 2024

Neural oscillations are associated with diverse computations in the mammalian brain. The waveform shape of oscillatory activity measured cortex relates to local physiology and can be informative about aberrant or dynamically changing states. However, how differs across distant yet functionally anatomically related cortical regions is largely unknown. In this study, we capitalize on simultaneous recordings field potentials (LFPs) auditory frontal cortices awake, male

Language: Английский

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Phase–Amplitude Coupling between Theta Rhythm and High-Frequency Oscillations in the Hippocampus of Pigeons during Navigation

Animals, Journal Year: 2024, Volume and Issue: 14(3), P. 439 - 439

Published: Jan. 29, 2024

Navigation is a complex task in which the hippocampus (Hp), plays an important role, may be involved interactions between different frequency bands. However, little known whether this cross-frequency interaction exists Hp of birds during navigation. Therefore, we examined electrophysiological characteristics hippocampal domestic pigeons (Columba livia domestica) Two goal-directed navigation tasks with locomotor modes were designed, and local field potentials (LFPs) recorded for analysis. We found that amplitudes high-frequency oscillations dynamically modulated by phase co-occurring theta-band both ground-based maze outdoor flight The amplitude sub-frequency bands theta at tasks, process was independent path goal. These results suggest phase–amplitude coupling (PAC) avian more associated ongoing cognitive demands navigational processes. Our findings contribute to understanding potential mechanisms PAC on multi-frequency informational provide valuable insights into cross-species evolution.

Language: Английский

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The pale spear‐nosed bat: A neuromolecular and transgenic model for vocal learning

Annals of the New York Academy of Sciences, Journal Year: 2022, Volume and Issue: 1517(1), P. 125 - 142

Published: Sept. 7, 2022

Abstract Vocal learning, the ability to produce modified vocalizations via learning from acoustic signals, is a key trait in evolution of speech. While extensively studied songbirds, mammalian models for vocal are rare. Bats present promising study system given their gregarious natures, small size, and some species be maintained captive colonies. We utilize pale spear‐nosed bat ( Phyllostomus discolor ) report advances establishing this as tractable model understanding learning. have taken an interdisciplinary approach, aiming provide integrated across genomics (Part I), neurobiology II), transgenics III). In Part I, we generated new, high‐quality genome annotations coding genes noncoding microRNAs facilitate functional evolutionary studies. II, traced connections between auditory‐related brain regions reported neuroimaging explore structure gene expression patterns highlight regions. III, created first successful transgenic bats by manipulating FoxP2 , speech‐related gene. These approaches facilitating mechanistic can also contribute other areas investigation that P. or species.

Language: Английский

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Oscillatory waveform shape and temporal spike correlations differ across bat frontal and auditory cortex

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: July 3, 2023

Abstract Neural oscillations are associated with diverse computations in the mammalian brain. The waveform shape of oscillatory activity measured cortex relates to local physiology, and can be informative about aberrant or dynamically changing states. However, how differs across distant yet functionally anatomically related cortical regions is largely unknown. In this study, we capitalize on simultaneous recordings field potentials (LFPs) auditory frontal cortices awake, male Carollia perspicillata bats examine, a cycle-by-cycle basis, differences regions. We find that markedly fronto-auditory circuit even for temporally correlated rhythmic comparable frequency ranges (i.e. delta gamma bands) during spontaneous activity. addition, report consistent between areas variability individual cycles. A conceptual model predicts higher spike-spike spike-LFP correlations more asymmetric shape, phenomenon was observed data: were cortex. suggests relationship spike areas. Altogether, these results indicate possess distinct dynamics anatomical functional diversity circuit. Significance statement brain many animals displays intricate oscillations, which usually characterized terms their amplitude. Here, study from bat additionally focusing characteristic shape. reveals clear regularity, when similar. waveforms result stronger neural spikes electrical Such predictions supported by data. findings shed light onto unique properties different areas, providing key insights into distinctive physiology within

Language: Английский

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Congenital Deafness Reduces Alpha-Gamma Cross-Frequency Coupling in the Auditory Cortex

Hearing Research, Journal Year: 2024, Volume and Issue: 449, P. 109032 - 109032

Published: May 17, 2024

Neurons within a neuronal network can be grouped by bottom-up and top-down influences using synchrony in oscillations. This creates the representation of perceptual objects from sensory features. Oscillatory activity differentiated into stimulus-phase-locked (evoked) non-phase-locked (induced). The former is mainly determined input, latter higher-level (cortical) processing. Effects auditory deprivation on cortical oscillations have been studied congenitally deaf cats (CDCs) cochlear implant (CI) stimulation. CI-induced alpha, beta, gamma were compromised cortex CDCs. Furthermore, information flow between secondary primary areas hearing cats, conveyed induced alpha oscillations, was lost Here we used matching pursuit algorithm to assess components such oscillatory local field potentials recorded A1. Additionally loss also found evoked theta CDCs directly related reduced high-frequency (gamma-band) due cross-frequency coupling. quantified coupling adult 1) hearing-experienced, acoustically stimulated (aHCs), 2) hearing-experienced following acute pharmacological deafening subsequent CIs, thus electrically (eHCs), 3) We significant all animal groups > 70% auditory-responsive sites. predominant aHCs eHCs theta/alpha phase power. In replaced delta/theta phase. Thus, alpha/theta synchronize only cats. absence contributes power CDCs, thereby signifying impaired activity.

Language: Английский

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Echolocation reverses information flow in a cortical vocalization network

Research Square (Research Square), Journal Year: 2021, Volume and Issue: unknown

Published: May 26, 2021

Abstract The mammalian frontal and auditory cortices are fundamental structures supporting vocal behaviour, yet the patterns of information exchange between these regions during vocalization remain unknown. Here, we address this issue by means electrophysiological recordings in fronto-auditory network freely-vocalizing Carollia perspicillata bats. We show that oscillations predict type with complementary across structures. Transfer entropy analyses oscillatory activity revealed directed circuit, predominantly top-down nature (frontal to auditory). dynamics flow depended on timing relative onset. Remarkably, observed emergence predominant bottom-up transfer, only when animals produced calls imminent post-vocal consequences (echolocation signals). These results unveil changes a large-scale sensory association associated behavioural highly model.

Language: Английский

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Echolocation reverses information flow in a cortical vocalization network

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2021, Volume and Issue: unknown

Published: March 15, 2021

Abstract The mammalian frontal and auditory cortices are important for vocal behaviour. Here, using local field potential recordings, we demonstrate the first time that timing spatial pattern of oscillations in fronto-auditory cortical network vocalizing bats ( Carollia perspicillata ) predict purpose vocalization: echolocation or communication. Transfer entropy analyses revealed predominantly top-down (frontal-to-auditory cortex) information flow during spontaneous activity pre-vocal periods. dynamics depended on behavioural role vocalization relative to onset. Remarkably, observed emergence bottom-up (auditory-to-frontal transfer patterns specific production, leading self-directed acoustic feedback. Electrical stimulation areas selectively enhanced responses sounds cortex. These results reveal unique changes across sensory cortices, potentially driven by a highly model.

Language: Английский

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