Detecting Spontaneous Neural Oscillation Events in Primate Auditory Cortex.

Electrophysiological oscillations in the brain have been shown to occur as multicycle events, with onset and offset dependent on behavioral and cognitive state. To provide a baseline for state-related and task-related events, we quantified oscillation features in resting-state recordings. We developed an open-source wavelet-based tool to detect and characterize such oscillation events (OEvents) and exemplify the use of this tool in both simulations and two invasively-recorded electrophysiology datasets: one from human, and one from nonhuman primate (NHP) auditory system. After removing incidentally occurring event-related potentials (ERPs), we used OEvents to quantify oscillation features. We identified ∼2 million oscillation events, classified within traditional frequency bands: δ, θ, α, ß, low γ, γ, and high γ. Oscillation events of 1-44 cycles could be identified in at least one frequency band 90% of the time in human and NHP recordings. Individual oscillation events were characterized by nonconstant frequency and amplitude. This result necessarily contrasts with prior studies which assumed frequency constancy, but is consistent with evidence from event-associated oscillations. We measured oscillation event duration, frequency span, and waveform shape. Oscillations tended to exhibit multiple cycles per event, verifiable by comparing filtered to unfiltered waveforms. In addition to the clear intraevent rhythmicity, there was also evidence of interevent rhythmicity within bands, demonstrated by finding that coefficient of variation of interval distributions and Fano factor (FF) measures differed significantly from a Poisson distribution assumption. Overall, our study provides an easy-to-use tool to study oscillation events at the single-trial level or in ongoing recordings, and demonstrates that rhythmic, multicycle oscillation events dominate auditory cortical dynamics.

Oscillatory Bursting as a Mechanism for Temporal Coupling and Information Coding.

Even the simplest cognitive processes involve interactions between cortical regions. To study these processes, we usually rely on averaging across several repetitions of a task or across long segments of data to reach a statistically valid conclusion. Neuronal oscillations reflect synchronized excitability fluctuations in ensembles of neurons and can be observed in electrophysiological recordings in the presence or absence of an external stimulus. Oscillatory brain activity has been viewed as sustained increase in power at specific frequency bands. However, this perspective has been challenged in recent years by the notion that oscillations may occur as transient burst-like events that occur in individual trials and may only appear as sustained activity when multiple trials are averaged together. In this review, we examine the idea that oscillatory activity can manifest as a transient burst as well as a sustained increase in power. We discuss the technical challenges involved in the detection and characterization of transient events at the single trial level, the mechanisms that might generate them and the features that can be extracted from these events to study single-trial dynamics of neuronal ensemble activity.

Dissociation of broadband high-frequency activity and neuronal firing in the neocortex.

Broadband high-frequency activity (BHA; 70 to 150 Hz), also known as "high gamma," a key analytic signal in human intracranial (electrocorticographic) recordings, is often assumed to reflect local neural firing [multiunit activity (MUA)]. As the precise physiological substrates of BHA are unknown, this assumption remains controversial. Our analysis of laminar multielectrode data from V1 and A1 in monkeys outlines two components of stimulus-evoked BHA distributed across the cortical layers: an "early-deep" and "late-superficial" response. Early-deep BHA has a clear spatial and temporal overlap with MUA. Late-superficial BHA was more prominent and accounted for more of the BHA signal measured near the cortical pial surface. However, its association with local MUA is weak and often undetectable, consistent with the view that it reflects dendritic processes separable from local neuronal firing.

Neural Entrainment to the Beat: The "Missing-Pulse" Phenomenon.

Most humans have a near-automatic inclination to tap, clap, or move to the beat of music. The capacity to extract a periodic beat from a complex musical segment is remarkable, as it requires abstraction from the temporal structure of the stimulus. It has been suggested that nonlinear interactions in neural networks result in cortical oscillations at the beat frequency, and that such entrained oscillations give rise to the percept of a beat or a pulse. Here we tested this neural resonance theory using MEG recordings as female and male individuals listened to 30 s sequences of complex syncopated drumbeats designed so that they contain no net energy at the pulse frequency when measured using linear analysis. We analyzed the spectrum of the neural activity while listening and compared it to the modulation spectrum of the stimuli. We found enhanced neural response in the auditory cortex at the pulse frequency. We also showed phase locking at the times of the missing pulse, even though the pulse was absent from the stimulus itself. Moreover, the strength of this pulse response correlated with individuals' speed in finding the pulse of these stimuli, as tested in a follow-up session. These findings demonstrate that neural activity at the pulse frequency in the auditory cortex is internally generated rather than stimulus-driven. The current results are both consistent with neural resonance theory and with models based on nonlinear response of the brain to rhythmic stimuli. The results thus help narrow the search for valid models of beat perception.SIGNIFICANCE STATEMENT Humans perceive music as having a regular pulse marking equally spaced points in time, within which musical notes are temporally organized. Neural resonance theory (NRT) provides a theoretical model explaining how an internal periodic representation of a pulse may emerge through nonlinear coupling between oscillating neural systems. After testing key falsifiable predictions of NRT using MEG recordings, we demonstrate the emergence of neural oscillations at the pulse frequency, which can be related to pulse perception. These findings rule out alternative explanations for neural entrainment and provide evidence linking neural synchronization to the perception of pulse, a widely debated topic in recent years.

Brain responses to regular and octave-scrambled melodies: A case of predictive-coding?

Melody recognition is an online process of evaluating incoming information and comparing this information to an existing internal corpus, thereby reducing prediction error. The predictive-coding model postulates top-down control on sensory processing accompanying reduction in prediction error. To investigate the relevancy of this model to melody processing, the current study examined early magnetoencephalogram (MEG) auditory responses to familiar and unfamiliar melodies in 25 participants. The familiar melodies followed and primed an octave-scrambled version of the same melody. The retrograde version of theses melodies served as the unfamiliar control condition. Octave-transposed melodies were included to examine the influence of pitch representation (pitch-height/pitch-chroma representation) on brain responses to melody recognition. Results demonstrate a reduction of the M100 auditory response to familiar, as compared with unfamiliar, melodies regardless of their form of presentation (condensed vs. octave-scrambled). This trend appeared to begin after the third tone of the melody. An additional behavioral study with the same melody corpus showed a similar trend-namely, a significant difference between familiarity rating for familiar and unfamiliar melodies, beginning with the third tone of the melody. These results may indicate a top-down inhibition of early auditory responses to melodies that is influenced by pitch representation. (PsycINFO Database Record

White matter microstructural properties correlate with sensorimotor synchronization abilities.

Sensorimotor synchronization (SMS) to an external auditory rhythm is a developed ability in humans, particularly evident in dancing and singing. This ability is typically measured in the lab via a simple task of finger tapping to an auditory beat. While simplistic, there is some evidence that poor performance on this task could be related to impaired phonological and reading abilities in children. Auditory-motor synchronization is hypothesized to rely on a tight coupling between auditory and motor neural systems, but the specific pathways that mediate this coupling have not been identified yet. In this study, we test this hypothesis and examine the contribution of fronto-temporal and callosal connections to specific measures of rhythmic synchronization. Twenty participants went through SMS and diffusion magnetic resonance imaging (dMRI) measurements. We quantified the mean asynchrony between an auditory beat and participants' finger taps, as well as the time to resynchronize (TTR) with an altered meter, and examined the correlations between these behavioral measures and diffusivity in a small set of predefined pathways. We found significant correlations between asynchrony and fractional anisotropy (FA) in the left (but not right) arcuate fasciculus and in the temporal segment of the corpus callosum. On the other hand, TTR correlated with FA in the precentral segment of the callosum. To our knowledge, this is the first demonstration that relates these particular white matter tracts with performance on an auditory-motor rhythmic synchronization task. We propose that left fronto-temporal and temporal-callosal fibers are involved in prediction and constant comparison between auditory inputs and motor commands, while inter-hemispheric connections between the motor/premotor cortices contribute to successful resynchronization of motor responses with a new external rhythm, perhaps via inhibition of tapping to the previous rhythm. Our results indicate that auditory-motor synchronization skills are associated with anatomical pathways that have been previously related to phonological awareness, thus offering a possible anatomical basis for the behavioral covariance between these abilities.

Temporal accuracy of human cortico-cortical interactions.

The precision in space and time of interactions among multiple cortical sites was evaluated by examining repeating precise spatiotemporal patterns of instances in which cortical currents showed brief amplitude undulations. The amplitudes of the cortical current dipoles were estimated by applying a variant of synthetic aperture magnetometry to magnetoencephalographic (MEG) recordings of subjects tapping to metric auditory rhythms of drum beats. Brief amplitude undulations were detected in the currents by template matching at a rate of 2-3 per second. Their timing was treated as point processes, and precise spatiotemporal patterns were searched for. By randomly teetering these point processes within a time window W, we estimated the accuracy of the timing of these brief amplitude undulations and compared the results with those obtained by applying the same analysis to traces composed of random numbers. The results demonstrated that the timing accuracy of patterns was better than 3 ms. Successful classification of two different cognitive processes based on these patterns suggests that at least some of the repeating patterns are specific to a cognitive process.