Oscillations In Auditory Cortex Research Articles

Dichotic listening deficits in amblyaudia are characterized by aberrant neural oscillations in auditory cortex

ObjectiveChildren diagnosed with auditory processing disorder (APD) show deficits in processing complex sounds that are associated with difficulties in higher-order language, learning, cognitive, and communicative functions. Amblyaudia (AMB) is a subcategory of APD characterized by abnormally large ear asymmetries in dichotic listening tasks. MethodsHere, we examined frequency-specific neural oscillations and functional connectivity via high-density electroencephalography (EEG) in children with and without AMB during passive listening of nonspeech stimuli. ResultsTime-frequency maps of these “brain rhythms” revealed stronger phase-locked beta-gamma (~35 Hz) oscillations in AMB participants within bilateral auditory cortex for sounds presented to the right ear, suggesting a hypersynchronization and imbalance of auditory neural activity. Brain-behavior correlations revealed neural asymmetries in cortical responses predicted the larger than normal right-ear advantage seen in participants with AMB. Additionally, we found weaker functional connectivity in the AMB group from right to left auditory cortex, despite their stronger neural responses overall. ConclusionOur results reveal abnormally large auditory sensory encoding and an imbalance in communication between cerebral hemispheres (ipsi- to -contralateral signaling) in AMB. SignificanceThese neurophysiological changes might lead to the functionally poorer behavioral capacity to integrate information between the two ears in children with AMB.

Converging intracortical signatures of two separated processing timescales in human early auditory cortex

Neural oscillations in auditory cortex are argued to support parsing and representing speech constituents at their corresponding temporal scales. Yet, how incoming sensory information interacts with ongoing spontaneous brain activity, what features of the neuronal microcircuitry underlie spontaneous and stimulus-evoked spectral fingerprints, and what these fingerprints entail for stimulus encoding, remain largely open questions. We used a combination of human invasive electrophysiology, computational modeling and decoding techniques to assess the information encoding properties of brain activity and to relate them to a plausible underlying neuronal microarchitecture. We analyzed intracortical auditory EEG activity from 10 patients while they were listening to short sentences. Pre-stimulus neural activity in early auditory cortical regions often exhibited power spectra with a shoulder in the delta range and a small bump in the beta range. Speech decreased power in the beta range, and increased power in the delta-theta and gamma ranges. Using multivariate machine learning techniques, we assessed the spectral profile of information content for two aspects of speech processing: detection and discrimination. We obtained better phase than power information decoding, and a bimodal spectral profile of information content with better decoding at low (delta-theta) and high (gamma) frequencies than at intermediate (beta) frequencies. These experimental data were reproduced by a simple rate model made of two subnetworks with different timescales, each composed of coupled excitatory and inhibitory units, and connected via a negative feedback loop. Modeling and experimental results were similar in terms of pre-stimulus spectral profile (except for the iEEG beta bump), spectral modulations with speech, and spectral profile of information content. Altogether, we provide converging evidence from both univariate spectral analysis and decoding approaches for a dual timescale processing infrastructure in human auditory cortex, and show that it is consistent with the dynamics of a simple rate model.

Implicit temporal predictability enhances pitch discrimination sensitivity and biases the phase of delta oscillations in auditory cortex

Can human listeners use implicit temporal contingencies in auditory input to form temporal predictions, and if so, how are these predictions represented endogenously? To assess this question, we implicitly manipulated temporal predictability in an auditory pitch discrimination task: unbeknownst to participants, the pitch of the standard tone could either be deterministically predictive of the temporal onset of the target tone, or convey no predictive information. Predictive and non-predictive conditions were presented interleaved in one stream, and separated by variable inter-stimulus intervals such that there was no dominant stimulus rhythm throughout. Even though participants were unaware of the implicit temporal contingencies, pitch discrimination sensitivity (the slope of the psychometric function) increased when the onset of the target tone was predictable in time (N = 49, 28 female, 21 male). Concurrently recorded EEG data (N = 24) revealed that standard tones that conveyed temporal predictions evoked a more negative N1 component than non-predictive standards. We observed no significant differences in oscillatory power or phase coherence between conditions during the foreperiod. Importantly, the phase angle of delta oscillations (1–3 Hz) in auditory areas in the post-standard and pre-target time windows predicted behavioral pitch discrimination sensitivity. This suggests that temporal predictions are encoded in delta oscillatory phase during the foreperiod interval. In sum, we show that auditory perception benefits from implicit temporal contingencies, and provide evidence for a role of slow neural oscillations in the endogenous representation of temporal predictions, in absence of exogenously driven entrainment to rhythmic input.

Beta oscillations in auditory cortex reflect temporal and spectral prediction in rhythmic contexts

Beta oscillations in auditory cortex reflect temporal and spectral prediction in rhythmic contexts

Unpredicted Pitch Modulates Beta Oscillatory Power during Rhythmic Entrainment to a Tone Sequence.

Extracting temporal regularities in external stimuli in order to predict upcoming events is an essential aspect of perception. Fluctuations in induced power of beta band (15–25 Hz) oscillations in auditory cortex are involved in predictive timing during rhythmic entrainment, but whether such fluctuations are affected by prediction in the spectral (frequency/pitch) domain remains unclear. We tested whether unpredicted (i.e., unexpected) pitches in a rhythmic tone sequence modulate beta band activity by recording EEG while participants passively listened to isochronous auditory oddball sequences with occasional unpredicted deviant pitches at two different presentation rates. The results showed that the power in low-beta (15–20 Hz) was larger around 200–300 ms following deviant tones compared to standard tones, and this effect was larger when the deviant tones were less predicted. Our results suggest that the induced beta power activities in auditory cortex are consistent with a role in sensory prediction of both “when” (timing) upcoming sounds will occur as well as the prediction precision error of “what” (spectral content in this case). We suggest, further, that both timing and content predictions may co-modulate beta oscillations via attention. These findings extend earlier work on neural oscillations by investigating the functional significance of beta oscillations for sensory prediction. The findings help elucidate the functional significance of beta oscillations in perception.

Endogenous Delta/Theta Sound-Brain Phase Entrainment Accelerates the Buildup of Auditory Streaming

In many natural listening situations, meaningful sounds (e.g., speech) fluctuate in slow rhythms among other sounds. When a slow rhythmic auditory stream is selectively attended, endogenous delta (1‒4 Hz) oscillations in auditory cortex may shift their timing so that higher-excitability neuronal phases become aligned with salient events in that stream [1, 2]. As a consequence of this stream-brain phase entrainment [3], these events are processed and perceived more readily than temporally non-overlapping events [4-11], essentially enhancing the neural segregation between the attended stream and temporally noncoherent streams [12]. Stream-brain phase entrainment is robust to acoustic interference [13-20] provided that target stream-evoked rhythmic activity can be segregated from noncoherent activity evoked by other sounds [21], a process that usually builds up over time [22-27]. However, it has remained unclear whether stream-brain phase entrainment functionally contributes to this buildup of rhythmic streams or whether it is merely an epiphenomenon of it. Here, we addressed this issue directly by experimentally manipulating endogenous stream-brain phase entrainment in human auditory cortex with non-invasive transcranial alternating current stimulation (TACS) [28-30]. We assessed the consequences of these manipulations on the perceptual buildup of the target stream (the time required to recognize its presence in a noisy background), using behavioral measures in 20 healthy listeners performing a naturalistic listening task. Experimentally induced cyclic 4-Hz variations in stream-brain phase entrainment reliably caused a cyclic 4-Hz pattern in perceptual buildup time. Our findings demonstrate that strong endogenous delta/theta stream-brain phase entrainment accelerates the perceptual emergence of task-relevant rhythmic streams in noisy environments.

Frontal Top-Down Signals Increase Coupling of Auditory Low-Frequency Oscillations to Continuous Speech in Human Listeners

SummaryHumans show a remarkable ability to understand continuous speech even under adverse listening conditions. This ability critically relies on dynamically updated predictions of incoming sensory information, but exactly how top-down predictions improve speech processing is still unclear. Brain oscillations are a likely mechanism for these top-down predictions [1, 2]. Quasi-rhythmic components in speech are known to entrain low-frequency oscillations in auditory areas [3, 4], and this entrainment increases with intelligibility [5]. We hypothesize that top-down signals from frontal brain areas causally modulate the phase of brain oscillations in auditory cortex. We use magnetoencephalography (MEG) to monitor brain oscillations in 22 participants during continuous speech perception. We characterize prominent spectral components of speech-brain coupling in auditory cortex and use causal connectivity analysis (transfer entropy) to identify the top-down signals driving this coupling more strongly during intelligible speech than during unintelligible speech. We report three main findings. First, frontal and motor cortices significantly modulate the phase of speech-coupled low-frequency oscillations in auditory cortex, and this effect depends on intelligibility of speech. Second, top-down signals are significantly stronger for left auditory cortex than for right auditory cortex. Third, speech-auditory cortex coupling is enhanced as a function of stronger top-down signals. Together, our results suggest that low-frequency brain oscillations play a role in implementing predictive top-down control during continuous speech perception and that top-down control is largely directed at left auditory cortex. This suggests a close relationship between (left-lateralized) speech production areas and the implementation of top-down control in continuous speech perception.

Mental structures and hierarchical brain processing: Comment on “Toward a computational framework for cognitive biology: Unifying approaches from cognitive neuroscience and comparative cognition” by W. Tecumseh Fitch

Fitch proposes an appealing hypothesis that humans are dendrophiles, who constantly build mental trees supported by analogous hierarchical brain processes [1]. Moreover, it is argued that, by comparison, nonhuman animals build flat or more compact behaviorally-relevant structures. Should we thus expect less impressive hierarchical brain processes in other animals? Not necessarily. Neuroscientific evidence is showing that the brains of humans and many animals are dendrophiles. The well-established notion of hierarchical brain processing was informed by human and nonhuman animal work [2,3]. Moreover, the form of processing is not just serial or parallel, because human, monkey and rodent brains have both local ‘small world’ connectivity patterns, as well as hubs that interconnect different ‘worlds’ [4]. Also, dendrograms as neuronal representations are prominent in a range of species: dendrograms can well describe monkey ventral frontal cortex neurons responding to vocalization sounds [5], and rodent hippocampal neurons can create multi-layered dendritic structures to encode several features associated with a memory [6]. In neither case is there any suggestion that different vocalizations or memory features are hierarchically organized by the animals for behavior. Also, hierarchically nested brain oscillations responding to speech are evident in humans [7], which is complemented by computational models of speech parsing [8]. Yet, nested oscillations are also evident in monkeys listening to natural sounds [9] and violations to a non-hierarchical artificial grammar that monkeys can learn appears to modulate nested oscillations in auditory cortex [10]. Much less clear, as Fitch suggests [1], is how to access the mental structures that humans and other animals sculpt. He suggests testing alternative hypotheses on the computations being conducted. For example, if one is evaluating strings generated by an AnBn grammar, different individuals might glean different structures depending on the mechanisms used, such as: (1) ‘push-down-stack’, where associations are computed and allocated to memory; or, (2) ‘count-and-compare’, where multiple counters keep track of the number of As and Bs (in the case of n = 3, 3 As and 3 Bs) and a comparison function evaluates whether they are equal. In the case of a ‘push-down-stack’, one might envision the human inferior frontal cortex associating different forms of input and holding the associations in memory. But it is unclear how this would differ or be informed by insights on hierarchically organized cognition in studies of neurons from monkey frontal cortex [11], or those on hierarchically organized memories in rodent fronto-hippocampal networks [6]. In the case of ‘count-and-compare’, this could be informed by numerosity encoding in monkey frontal neurons [12]. The danger, however, which Fitch does not appear to condone, is overlooking the insights that we can gain from nonhuman animals if most are viewed as having, at least by human standards, unsophisticated mental structures. I agree that a priority is for hypotheses to be better developed and tested on the computations subserving different behaviorally-relevant structures, which even in humans has remained largely theoretical. Each computational hypothesis supported or refuted clarifies the types of structures being built by an individual or their species. Neurobiological evidence can provide mechanistic insights. However, it is incorrect to assume that hierarchical neural processes subserve only hierarchical representations of the forms that humans uniquely can build. After all, it is already abundantly clear that the brains of most animals like building elaborate structures.

Acoustic landmarks drive delta–theta oscillations to enable speech comprehension by facilitating perceptual parsing

A growing body of research suggests that intrinsic neuronal slow (<10Hz) oscillations in auditory cortex appear to track incoming speech and other spectro-temporally complex auditory signals. Within this framework, several recent studies have identified critical-band temporal envelopes as the specific acoustic feature being reflected by the phase of these oscillations. However, how this alignment between speech acoustics and neural oscillations might underpin intelligibility is unclear. Here we test the hypothesis that the ‘sharpness’ of temporal fluctuations in the critical band envelope acts as a temporal cue to speech syllabic rate, driving delta–theta rhythms to track the stimulus and facilitate intelligibility. We interpret our findings as evidence that sharp events in the stimulus cause cortical rhythms to re-align and parse the stimulus into syllable-sized chunks for further decoding. Using magnetoencephalographic recordings, we show that by removing temporal fluctuations that occur at the syllabic rate, envelope-tracking activity is reduced. By artificially reinstating these temporal fluctuations, envelope-tracking activity is regained. These changes in tracking correlate with intelligibility of the stimulus. Together, the results suggest that the sharpness of fluctuations in the stimulus, as reflected in the cochlear output, drive oscillatory activity to track and entrain to the stimulus, at its syllabic rate. This process likely facilitates parsing of the stimulus into meaningful chunks appropriate for subsequent decoding, enhancing perception and intelligibility.

Single-subject oscillatory gamma responses in tinnitus

This study used magnetoencephalography to record oscillatory activity in a group of 17 patients with chronic tinnitus. Two methods, residual inhibition and residual excitation, were used to bring about transient changes in spontaneous tinnitus intensity in order to measure dynamic tinnitus correlates in individual patients. In residual inhibition, a positive correlation was seen between tinnitus intensity and both delta/theta (6/14 patients) and gamma band (8/14 patients) oscillations in auditory cortex, suggesting an increased thalamocortical input and cortical gamma response, respectively, associated with higher tinnitus states. Conversely, 4/4 patients exhibiting residual excitation demonstrated an inverse correlation between perceived tinnitus intensity and auditory cortex gamma oscillations (with no delta/theta changes) that cannot be explained by existing models. Significant oscillatory power changes were also identified in a variety of cortical regions, most commonly midline lobar regions in the default mode network, cerebellum, insula and anterior temporal lobe. These were highly variable across patients in terms of areas and frequency bands involved, and in direction of power change. We suggest a model based on a local circuit function of cortical gamma-band oscillations as a process of mutual inhibition that might suppress abnormal cortical activity in tinnitus. The work implicates auditory cortex gamma-band oscillations as a fundamental intrinsic mechanism for attenuating phantom auditory perception.

Phase-Locked Responses to Speech in Human Auditory Cortex are Enhanced During Comprehension

A growing body of evidence shows that ongoing oscillations in auditory cortex modulate their phase to match the rhythm of temporally regular acoustic stimuli, increasing sensitivity to relevant environmental cues and improving detection accuracy. In the current study, we test the hypothesis that nonsensory information provided by linguistic content enhances phase-locked responses to intelligible speech in the human brain. Sixteen adults listened to meaningful sentences while we recorded neural activity using magnetoencephalography. Stimuli were processed using a noise-vocoding technique to vary intelligibility while keeping the temporal acoustic envelope consistent. We show that the acoustic envelopes of sentences contain most power between 4 and 7 Hz and that it is in this frequency band that phase locking between neural activity and envelopes is strongest. Bilateral oscillatory neural activity phase-locked to unintelligible speech, but this cerebro-acoustic phase locking was enhanced when speech was intelligible. This enhanced phase locking was left lateralized and localized to left temporal cortex. Together, our results demonstrate that entrainment to connected speech does not only depend on acoustic characteristics, but is also affected by listeners’ ability to extract linguistic information. This suggests a biological framework for speech comprehension in which acoustic and linguistic cues reciprocally aid in stimulus prediction.

Word repetition priming-induced oscillations in auditory cortex

Magnetoencephalography was used in a passive repetition priming paradigm. Words in two frequency bins (high/low) were presented to the participants auditorily. Participants' brain responses to these stimuli were analyzed using synthetic aperture magnetometry. The main finding of this study is that single-word repetition of low-frequency word pairs significantly attenuated the post-second word event-related desynchronization in the θ-α (5-15 Hz) bands, at 200-600 ms of post-second word stimulus onset. Peak significance between repeated high and low frequency words was evident at approximately 365-465 ms of posttarget onset. This finding has implications for: (i) the role of θ-α event-related desynchronization in lexical representation and access, (ii) the study of repetition suppression in the spectral-temporal domain, and (iii) the connection of neuronal repetition suppression with behavioral effects of repetition priming.

The Multisensory Nature of Unisensory Cortices: A Puzzle Continued

Multisensory integration is central to perception, and recent work drafts it as a distributed process involving many and even primary sensory cortices. Studies in behaving animals performing a multisensory task provide an ideal means to elucidate the underlying neural basis, and a new study by Lemus et al. in this issue of Neuron thrusts in this direction.

Sensorimotor and auditory cortical activity during passive listening to rhythmic tone sequences

Event Abstract Back to Event Sensorimotor and auditory cortical activity during passive listening to rhythmic tone sequences Paul Ferrari1*, Douglas Cheyne1, 2, Kelly Jantzen3, Scott J. Kelso4 and Armin Fuchs4 1 The Hospital for Sick Children, Program in Neurosciences and Mental Health, Canada 2 University of Toronto, Department of Medical Imaging, Canada 3 Western Washington University, Department of Psychology, United States 4 Florida Atlantic University, Center for Complex Systems and Brain Sciences, United States The perception of rhythmic events is inextricably linked to the ability to coordinate with the external world, e.g. music perception and dance. Recent neuroimaging studies have found that auditory rhythm perception is supported by numerous extra-auditory sources, including sensorimotor cortex (SMC) [1]. Surface recordings using EEG/MEG have been used to measure the spectro-temporal profiles of event-related oscillatory activity during rhythmic processing [2,3]. However, a mapping of these temporal profiles onto their underlying generators is lacking. Using MEG beamforming we localized cortical sources of neuromagnetic activity in 7 subjects during passive listening to isochronic pure tone stimuli at three different rates. Auditory cortex (AC) sources were localized in all subjects. A contrast between pre- and post-stimulus beta-band (15-30Hz) activity revealed focal peaks of desynchronization in SMC in 6 subjects. Event-related volumetric images revealed activity in AC and extra-auditory regions prior to stimulus onset, tracked neural propagation from AC to SMC, with a peak of activity occurring in supplementary motor cortex at approximately 300ms post stimulus. Time-frequency analysis showed modulations of beta-gamma oscillations that depended on stimulation rate. At slow stimulus rates (0.75Hz), beta-gamma oscillations in AC synchronized around stimulus onset while SMC sources desynchronized. At the highest rate of stimulus presentation (1.75Hz), cortical oscillation patterns became complex, possibly due to overlapping oscillatory rebound processes. The results support the role of SMC in the processing of temporally-structured auditory events and motivate future studies of multi-modal processes during sensorimotor coordination.

Cellular mechanisms of thalamically evoked gamma oscillations in auditory cortex.

The purpose of this study was to clarify the neurogenesis of thalamically evoked gamma frequency (approximately 40 Hz) oscillations in auditory cortex by comparing simultaneously recorded extracellular and intracellular responses elicited with electrical stimulation of the posterior intralaminar nucleus of the thalamus (PIL). The focus of evoked gamma activity was located between primary and secondary auditory cortex using a 64-channel epipial electrode array, and all subsequent intracellular recordings and single-electrode field potential recordings were made at this location. These data indicate that PIL stimulation evokes gamma oscillations in auditory cortex by tonically depolarizing pyramidal cells in the supra- and infragranular layers. No cells revealed endogenous membrane properties capable of producing activity in the gamma frequency band when depolarized individually with injected current, but all displayed both sub- and supra-threshold responses time-locked to extracellular fast oscillations when the population was depolarized by PIL stimulation. We propose that cortical gamma oscillations may be produced and propagated intracortically by network interactions among large groups of neurons when mutually excited by modulatory input from the intralaminar thalamus and that these oscillations do not require specialized pacemaker cells for their neurogenesis.

Three-dimensional analysis of spontaneous and thalamically evoked gamma oscillations in auditory cortex.

The purpose of this study was to investigate interactions among laminar cell populations producing spontaneous and evoked high-frequency (approximately 40 Hz) gamma oscillations in auditory cortex. Electrocortical oscillations were recorded using a 64-channel epipial electrode array and a 16-channel linear laminar electrode array while electrical stimulation was delivered to the posterior intralaminar (PIL) nucleus. Spontaneous gamma oscillations, and those evoked by PIL stimulation, are confined to a location overlapping primary and secondary auditory cortex. Current source-density and principal components analysis of laminar recordings at this site indicate that the auditory evoked potential (AEP) complex is characterized by a stereotyped asynchronous activation of supra- and infragranular cell populations. Similar analysis of spontaneous and evoked gamma waves reveals a close spatiotemporal similarity to the laminar AEP, indicating rhythmic interactions between supra- and infragranular cell groups during these oscillatory phenomena. We conclude that neural circuit interactions producing the laminar AEP onset in auditory cortex are the same as those generating evoked and spontaneous gamma oscillations.

Subcortical modulation of high-frequency (gamma band) oscillating potentials in auditory cortex.

The purpose of this study was to use depth electrical stimulation and retrograde horseradish peroxidase (HRP) labeling to determine what role certain subcortical nuclei play in the neurogenesis of high-frequency gamma (approximately 40 Hz) oscillations in rat auditory cortex. Evoked and spontaneous electrocortical oscillations were recorded with the use of a high-spatial-resolution multichannel epipial electrode array while electrical stimulation was delivered to the posterior intralaminar (PIL) region of the ventral acoustic thalamus and to the centrolateral nucleus (CL) and the nucleus basalis (NB), which have been previously implicated in the production of cortical gamma oscillations. PIL stimulation consistently evoked gamma oscillations confined to a location between primary and secondary auditory cortex, corresponding to the region where spontaneous gamma oscillations were also recorded. Stimulation of the CL and NB did not evoke gamma oscillations in auditory cortex. HRP placed in the cortical focus of evoked gamma oscillations labeled cell bodies in the PIL, and in more lateral regions of the ventral acoustic thalamus, which on subsequent stimulation also evoked gamma oscillations in auditory cortex. No cells were labeled in either the CL or NB. These results indicate that the PIL and the lateral regions of ventral acoustic thalamus provide anatomically distinct input to auditory cortex and may play an exclusive and modality-specific role in modulating gamma oscillations in the auditory system.

Thalamic modulation of high-frequency oscillating potentials in auditory cortex.

Perhaps the most widely recognized but least understood electrophysiological activity of the cerebral cortex is its characteristic electrical oscillations. Recently, there have been efforts to understand the mechanisms underlying high-frequency gamma oscillations(approximately 40 Hz) because they may coordinate sensory processing between populations of cortical cells. High-resolution cortical recordings show the gamma oscillations are constrained to sensory cortex, that they occur independently in auditory and somatosensory cortex, and that they are phase-locked between primary and secondary sensory cortex. As yet, the mechanism of their neurogenesis is unknown. Whereas cortical neurons can produce gamma oscillations without subcortical input, they may also be modulated by the thalamus and basal forebrain. Here we report that the neural generator of gamma oscillations in auditory cortex seems to be intracortical, serving to synchronize interactions between the primary and secondary areas. The acoustic thalamus directly modulates these oscillations, which are inhibited by stimulation of the dorsal and ventral divisions of the medial geniculate nucleus (MGd and MGv) and evoked by stimulation of the adjacent posterior intralaminar nucleus (PIL).