Activity In Human Auditory Cortex Research Articles

Visual Stimuli Modulate Local Field Potentials But Drive No High-Frequency Activity in Human Auditory Cortex.

Neuroimaging studies suggest cross-sensory visual influences in human auditory cortices (ACs). Whether these influences reflect active visual processing in human ACs, which drives neuronal firing and concurrent broadband high-frequency activity (BHFA; >70 Hz), or whether they merely modulate sound processing is still debatable. Here, we presented auditory, visual, and audiovisual stimuli to 16 participants (7 women, 9 men) with stereo-EEG depth electrodes implanted near ACs for presurgical monitoring. Anatomically normalized group analyses were facilitated by inverse modeling of intracranial source currents. Analyses of intracranial event-related potentials (iERPs) suggested cross-sensory responses to visual stimuli in ACs, which lagged the earliest auditory responses by several tens of milliseconds. Visual stimuli also modulated the phase of intrinsic low-frequency oscillations and triggered 15-30 Hz event-related desynchronization in ACs. However, BHFA, a putative correlate of neuronal firing, was not significantly increased in ACs after visual stimuli, not even when they coincided with auditory stimuli. Intracranial recordings demonstrate cross-sensory modulations, but no indication of active visual processing in human ACs.

Two stages of speech envelope tracking in human auditory cortex modulated by speech intelligibility.

The envelope is essential for speech perception. Recent studies have shown that cortical activity can track the acoustic envelope. However, whether the tracking strength reflects the extent of speech intelligibility processing remains controversial. Here, using stereo-electroencephalogram technology, we directly recorded the activity in human auditory cortex while subjects listened to either natural or noise-vocoded speech. These 2 stimuli have approximately identical envelopes, but the noise-vocoded speech does not have speech intelligibility. According to the tracking lags, we revealed 2 stages of envelope tracking: an early high-γ (60-140Hz) power stage that preferred the noise-vocoded speech and a late θ (4-8Hz) phase stage that preferred the natural speech. Furthermore, the decoding performance of high-γ power was better in primary auditory cortex than in nonprimary auditory cortex, consistent with its short tracking delay, while θ phase showed better decoding performance in right auditory cortex. In addition, high-γ responses with sustained temporal profiles in nonprimary auditory cortex were dominant in both envelope tracking and decoding. In sum, we suggested a functional dissociation between high-γ power and θ phase: the former reflects fast and automatic processing of brief acoustic features, while the latter correlates to slow build-up processing facilitated by speech intelligibility.

Hemispheric decoupling of awareness-related activity in human auditory cortex under informational masking and divided attention

Whether unattended sound streams reach perceptual awareness, and the extent to which they are represented in the central auditory system, are fundamental questions of modern hearing science. We examined these questions utilizing M/EEG, multi-tone masking, and a dual-task dichotic listening paradigm. Listeners performed a demanding primary task in one ear—detecting isochronous target-tone streams embedded in random multi-tone backgrounds and counting within-target-stream deviants—and retrospectively reported their awareness of similar masker-embedded targets in the other ear. Irrespective of attention or stimulation ear, left-AC activity strongly covaried with target-stream detection starting as early as 50 ms post-stimulus. In contrast, right-AC activity, while highly sensitive to stimulation ear, was unmodulated by detection until later, and then only weakly. Thus, under certain conditions, human ACs can functionally decouple, such that one—here, right—is automatic and stimulus-driven while the other—here, left—supports perceptual and/or task demands, including basic perceptual awareness of nonverbal sounds both within and outside the focus of top-down selective attention.

Activity in Human Auditory Cortex Represents Spatial Separation Between Concurrent Sounds.

The primary and posterior auditory cortex (AC) are known for their sensitivity to spatial information, but how this information is processed is not yet understood. AC that is sensitive to spatial manipulations is also modulated by the number of auditory streams present in a scene (Smith et al., 2010), suggesting that spatial and nonspatial cues are integrated for stream segregation. We reasoned that, if this is the case, then it is the distance between sounds rather than their absolute positions that is essential. To test this hypothesis, we measured human brain activity in response to spatially separated concurrent sounds with fMRI at 7 tesla in five men and five women. Stimuli were spatialized amplitude-modulated broadband noises recorded for each participant via in-ear microphones before scanning. Using a linear support vector machine classifier, we investigated whether sound location and/or location plus spatial separation between sounds could be decoded from the activity in Heschl's gyrus and the planum temporale. The classifier was successful only when comparing patterns associated with the conditions that had the largest difference in perceptual spatial separation. Our pattern of results suggests that the representation of spatial separation is not merely the combination of single locations, but rather is an independent feature of the auditory scene.SIGNIFICANCE STATEMENT Often, when we think of auditory spatial information, we think of where sounds are coming from-that is, the process of localization. However, this information can also be used in scene analysis, the process of grouping and segregating features of a soundwave into objects. Essentially, when sounds are further apart, they are more likely to be segregated into separate streams. Here, we provide evidence that activity in the human auditory cortex represents the spatial separation between sounds rather than their absolute locations, indicating that scene analysis and localization processes may be independent.

Activity in human auditory cortex represents spatial separation between concurrent sounds

Auditory spatial information can enhance stream segregation in an auditory scene, but little is known about how auditory space is represented in the human cortex. If spatial cues are used for scene analysis, then it is the distance between sounds rather than their absolute positions that is essential, and thus, we hypothesized that auditory cortical neurons encode separation between sounds rather than absolute location. To test this hypothesis, we measured human brain activity in response to spatially-separated concurrent sounds with magnetic resonance imaging at 7 Tesla. Stimuli were spatialized amplitude-modulated broadband noises, recorded for each participant via in-ear microphones prior to scanning. Using a linear support vector machine classifier, we investigated if sound location and/or spatial separation between sounds could be decoded from the activity in Heschl's gyrus and the planum temporale. The classifier was successful only when comparing patterns associated with the conditions that had the largest difference in perceptual spatial separation, and not in conditions where only location changed and separation remained constant. Our pattern of results suggest that the representation of separation is not merely the combination of single locations, but is an independent feature of the auditory scene.

Interaction of streaming and attention in human auditory cortex.

Serially presented tones are sometimes segregated into two perceptually distinct streams. An ongoing debate is whether this basic streaming phenomenon reflects automatic processes or requires attention focused to the stimuli. Here, we examined the influence of focused attention on streaming-related activity in human auditory cortex using magnetoencephalography (MEG). Listeners were presented with a dichotic paradigm in which left-ear stimuli consisted of canonical streaming stimuli (ABA_ or ABAA) and right-ear stimuli consisted of a classical oddball paradigm. In phase one, listeners were instructed to attend the right-ear oddball sequence and detect rare deviants. In phase two, they were instructed to attend the left ear streaming stimulus and report whether they heard one or two streams. The frequency difference (ΔF) of the sequences was set such that the smallest and largest ΔF conditions generally induced one- and two-stream percepts, respectively. Two intermediate ΔF conditions were chosen to elicit bistable percepts (i.e., either one or two streams). Attention enhanced the peak-to-peak amplitude of the P1-N1 complex, but only for ambiguous ΔF conditions, consistent with the notion that automatic mechanisms for streaming tightly interact with attention and that the latter is of particular importance for ambiguous sound sequences.

Acoustical and categorical tasks differently modulate activations of human auditory cortex to vowels

The present study compared activations to prototype, nonprototype, nonphonemic, and cross-category vowel pairs during vowel discrimination, category discrimination, 2-back, and visual tasks. Our results support previous findings that areas of the superior temporal gyrus (STG) are sensitive to the speech-level difference between prototype vs. nonprototype and phonemic vs. nonphonemic vowels. Further, consistent with previous studies, we found enhanced activations in anterior-posterior STG and inferior parietal lobule (IPL) during the vowel discrimination and 2-back tasks, respectively. Unlike the vowel discrimination task, the category discrimination task was associated with strong IPL activations. Our results provide evidence that activations in STG and IPL strongly depend on whether the task requires analysis of detailed acoustical information or operations on categorical representations. Based on previous studies investigating activations during categorical pitch and spatial tasks, we argue that this distinction is probably not specific to speech.

Source Analysis of Event-Related Potentials During Pitch Discrimination and Pitch Memory Tasks

Our previous studies using fMRI have demonstrated that activations in human auditory cortex (AC) are strongly dependent on the characteristics of the task. The present study tested whether source estimation of scalp-recorded event-related potentials (ERPs) can be used to investigate task-dependent AC activations. Subjects were presented with frequency-varying two-part tones during pitch discrimination, pitch n-back memory, and visual tasks identical to our previous fMRI study (Rinne et al., J Neurosci 29:13338-13343, 2009). ERPs and their minimum-norm source estimates in AC were strongly modulated by task at 200-700ms from tone onset. As in the fMRI study, the pitch discrimination and pitch memory tasks were associated with distinct AC activation patterns. In the pitch discrimination task, increased activity in the anterior AC was detected relatively late at 300-700ms from tone onset. Therefore, this activity was probably not associated with enhanced pitch processing but rather with the actual discrimination process (comparison between the two parts of tone). Increased activity in more posterior areas associated with the pitch memory task, in turn, occurred at 200-700ms suggesting that this activity was related to operations on pitch categories after pitch analysis was completed. Finally, decreased activity associated with the pitch memory task occurred at 150-300ms consistent with the notion that, in the demanding pitch memory task, spectrotemporal analysis is actively halted as soon as category information has been obtained. These results demonstrate that ERP source analysis can be used to complement fMRI to investigate task-dependent activations of human AC.

Perceptual Demand Modulates Activation of Human Auditory Cortex in Response to Task-irrelevant Sounds

In the visual modality, perceptual demand on a goal-directed task has been shown to modulate the extent to which irrelevant information can be disregarded at a sensory-perceptual stage of processing. In the auditory modality, the effect of perceptual demand on neural representations of task-irrelevant sounds is unclear. We compared simultaneous ERPs and fMRI responses associated with task-irrelevant sounds across parametrically modulated perceptual task demands in a dichotic-listening paradigm. Participants performed a signal detection task in one ear (Attend ear) while ignoring task-irrelevant syllable sounds in the other ear (Ignore ear). Results revealed modulation of syllable processing by auditory perceptual demand in an ROI in middle left superior temporal gyrus and in negative ERP activity 130-230 msec post stimulus onset. Increasing the perceptual demand in the Attend ear was associated with a reduced neural response in both fMRI and ERP to task-irrelevant sounds. These findings are in support of a selection model whereby ongoing perceptual demands modulate task-irrelevant sound processing in auditory cortex.

Activations of human auditory cortex to phonemic and nonphonemic vowels during discrimination and memory tasks

We used fMRI to investigate activations within human auditory cortex (AC) to vowels during vowel discrimination, vowel (categorical n-back) memory, and visual tasks. Based on our previous studies, we hypothesized that the vowel discrimination task would be associated with increased activations in the anterior superior temporal gyrus (STG), while the vowel memory task would enhance activations in the posterior STG and inferior parietal lobule (IPL). In particular, we tested the hypothesis that activations in the IPL during vowel memory tasks are associated with categorical processing. Namely, activations due to categorical processing should be higher during tasks performed on nonphonemic (hard to categorize) than on phonemic (easy to categorize) vowels. As expected, we found distinct activation patterns during vowel discrimination and vowel memory tasks. Further, these task-dependent activations were different during tasks performed on phonemic or nonphonemic vowels. However, activations in the IPL associated with the vowel memory task were not stronger during nonphonemic than phonemic vowel blocks. Together these results demonstrate that activations in human AC to vowels depend on both the requirements of the behavioral task and the phonemic status of the vowels.

The Tracking of Speech Envelope in the Human Cortex

Humans are highly adept at processing speech. Recently, it has been shown that slow temporal information in speech (i.e., the envelope of speech) is critical for speech comprehension. Furthermore, it has been found that evoked electric potentials in human cortex are correlated with the speech envelope. However, it has been unclear whether this essential linguistic feature is encoded differentially in specific regions, or whether it is represented throughout the auditory system. To answer this question, we recorded neural data with high temporal resolution directly from the cortex while human subjects listened to a spoken story. We found that the gamma activity in human auditory cortex robustly tracks the speech envelope. The effect is so marked that it is observed during a single presentation of the spoken story to each subject. The effect is stronger in regions situated relatively early in the auditory pathway (belt areas) compared to other regions involved in speech processing, including the superior temporal gyrus (STG) and the posterior inferior frontal gyrus (Broca's region). To further distinguish whether speech envelope is encoded in the auditory system as a phonological (speech-related), or instead as a more general acoustic feature, we also probed the auditory system with a melodic stimulus. We found that belt areas track melody envelope weakly, and as the only region considered. Together, our data provide the first direct electrophysiological evidence that the envelope of speech is robustly tracked in non-primary auditory cortex (belt areas in particular), and suggest that the considered higher-order regions (STG and Broca's region) partake in a more abstract linguistic analysis.

Task‐dependent activations of human auditory cortex to prototypical and nonprototypical vowels

Research in auditory neuroscience has largely neglected the possible effects of different listening tasks on activations of auditory cortex (AC). In the present study, we used high-resolution fMRI to compare human AC activations with sounds presented during three auditory and one visual task. In all tasks, subjects were presented with pairs of Finnish vowels, noise bursts with pitch and Gabor patches. In the vowel pairs, one vowel was always either a prototypical /i/ or /ae/ (separately defined for each subject) or a nonprototype. In different task blocks, subjects were either required to discriminate (same/different) vowel pairs, to rate vowel "goodness" (first/second sound was a better exemplar of the vowel class), to discriminate pitch changes in the noise bursts, or to discriminate Gabor orientation changes. We obtained distinctly different AC activation patterns to identical sounds presented during the four task conditions. In particular, direct comparisons between the vowel tasks revealed stronger activations during vowel discrimination in the anterior and posterior superior temporal gyrus (STG), while the vowel rating task was associated with increased activations in the inferior parietal lobule (IPL). We also found that AC areas in or near Heschl's gyrus (HG) were sensitive to the speech-specific difference between a vowel prototype and nonprototype during active listening tasks. These results show that AC activations to speech sounds are strongly dependent on the listening tasks.

Task-dependent activations of human auditory cortex during spatial discrimination and spatial memory tasks

In the present study, we applied high-resolution functional magnetic resonance imaging (fMRI) of the human auditory cortex (AC) and adjacent areas to compare activations during spatial discrimination and spatial n-back memory tasks that were varied parametrically in difficulty. We found that activations in the anterior superior temporal gyrus (STG) were stronger during spatial discrimination than during spatial memory, while spatial memory was associated with stronger activations in the inferior parietal lobule (IPL). We also found that wide AC areas were strongly deactivated during the spatial memory tasks. The present AC activation patterns associated with spatial discrimination and spatial memory tasks were highly similar to those obtained in our previous study comparing AC activations during pitch discrimination and pitch memory (Rinne et al., 2009). Together our previous and present results indicate that discrimination and memory tasks activate anterior and posterior AC areas differently and that this anterior-posterior division is present both when these tasks are performed on spatially invariant (pitch discrimination vs. memory) or spatially varying (spatial discrimination vs. memory) sounds. These results also further strengthen the view that activations of human AC cannot be explained only by stimulus-level parameters (e.g., spatial vs. nonspatial stimuli) but that the activations observed with fMRI are strongly dependent on the characteristics of the behavioral task. Thus, our results suggest that in order to understand the functional structure of AC a more systematic investigation of task-related factors affecting AC activations is needed.

Invariance of firing rate and field potential dynamics to stimulus modulation rate in human auditory cortex

The effect of stimulus modulation rate on the underlying neural activity in human auditory cortex is not clear. Human studies (using both invasive and noninvasive techniques) have demonstrated that at the population level, auditory cortex follows stimulus envelope. Here we examined the effect of stimulus modulation rate by using a rare opportunity to record both spiking activity and local field potentials (LFP) in auditory cortex of patients during repeated presentations of an audio-visual movie clip presented at normal, double, and quadruple speeds. Mean firing rate during evoked activity remained the same across speeds and the temporal response profile of firing rate modulations at increased stimulus speeds was a linearly scaled version of the response during slower speeds. Additionally, stimulus induced power modulation of local field potentials in the high gamma band (64-128 Hz) exhibited similar temporal scaling as the neuronal firing rate modulations. Our data confirm and extend previous studies in humans and anesthetized animals, supporting a model in which both firing rate, and high-gamma LFP power modulations in auditory cortex follow the temporal envelope of the stimulus across different modulation rates.

Task-dependent activations of human auditory cortex during non-spatial and spatial tasks

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Activations of Human Auditory Cortex During Visual and Auditory Selective Attention Tasks with Varying Difficulty

The present study was designed to directly test the hypothesis that suppression of activations to task-irrelevant sounds contributes to the attention-related modulations of auditory cortex (AC) activations observed in previous fMRI studies. Subjects selectively attended to auditory (broadband noise bursts with pitch) or visual (Gabor gratings) asynchronous fast-rate stimulus streams concurrently presented to left-ear, right-ear, above-fixation, or below-fixation. Auditory and visual task difficulty was parametrically manipulated in three levels. Behavioral data obtained during fMRI indicated that subjects achieved acceptable performance levels in all tasks and that the task-difficulty manipulation was effective. Consistent with previous studies, AC activations strongly depended on the direction of attention. AC activations to sounds were higher during auditory than during visual tasks and AC activations were higher in the hemisphere contralateral to the attended ear. However, the effects of task difficulty on AC activations were weak or non-existent. In particular, increasing task difficulty was not associated with a systematic decrease of AC activations in areas that were modulated by attention. These results suggest that suppression of AC activations to task-irrelevant sounds is likely to be small or negligible as compared with the strong activation enhancements observed in fMRI during active auditory tasks.

Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category

How the brain processes complex sounds, like voices or musical instrument sounds, is currently not well understood. The features comprising the acoustic profiles of such sounds are thought to be represented by neurons responding to increasing degrees of complexity throughout auditory cortex, with complete auditory "objects" encoded by neurons (or small networks of neurons) in anterior superior temporal regions. Although specialized voice and speech-sound regions have been proposed, it is unclear how other types of complex natural sounds are processed within this object-processing pathway. Using functional magnetic resonance imaging, we sought to demonstrate spatially distinct patterns of category-selective activity in human auditory cortex, independent of semantic content and low-level acoustic features. Category-selective responses were identified in anterior superior temporal regions, consisting of clusters selective for musical instrument sounds and for human speech. An additional subregion was identified that was particularly selective for the acoustic-phonetic content of speech. In contrast, regions along the superior temporal plane closer to primary auditory cortex were not selective for stimulus category, responding instead to specific acoustic features embedded in natural sounds, such as spectral structure and temporal modulation. Our results support a hierarchical organization of the anteroventral auditory-processing stream, with the most anterior regions representing the complete acoustic signature of auditory objects.

Bottom-Up Driven Involuntary Auditory Evoked Field Change: Constant Sound Sequencing Amplifies But Does Not Sharpen Neural Activity

The capability of involuntarily tracking certain sound signals during the simultaneous presence of noise is essential in human daily life. Previous studies have demonstrated that top-down auditory focused attention can enhance excitatory and inhibitory neural activity, resulting in sharpening of frequency tuning of auditory neurons. In the present study, we investigated bottom-up driven involuntary neural processing of sound signals in noisy environments by means of magnetoencephalography. We contrasted two sound signal sequencing conditions: "constant sequencing" versus "random sequencing." Based on a pool of 16 different frequencies, either identical (constant sequencing) or pseudorandomly chosen (random sequencing) test frequencies were presented blockwise together with band-eliminated noises to nonattending subjects. The results demonstrated that the auditory evoked fields elicited in the constant sequencing condition were significantly enhanced compared with the random sequencing condition. However, the enhancement was not significantly different between different band-eliminated noise conditions. Thus the present study confirms that by constant sound signal sequencing under nonattentive listening the neural activity in human auditory cortex can be enhanced, but not sharpened. Our results indicate that bottom-up driven involuntary neural processing may mainly amplify excitatory neural networks, but may not effectively enhance inhibitory neural circuits.

Task-Dependent Activations of Human Auditory Cortex during Pitch Discrimination and Pitch Memory Tasks

The functional organization of auditory cortex (AC) is still poorly understood. Previous studies suggest segregation of auditory processing streams for spatial and nonspatial information located in the posterior and anterior AC, respectively (Rauschecker and Tian, 2000; Arnott et al., 2004; Lomber and Malhotra, 2008). Furthermore, previous studies have shown that active listening tasks strongly modulate AC activations (Petkov et al., 2004; Fritz et al., 2005; Polley et al., 2006). However, the task dependence of AC activations has not been systematically investigated. In the present study, we applied high-resolution functional magnetic resonance imaging of the AC and adjacent areas to compare activations during pitch discrimination and n-back pitch memory tasks that were varied parametrically in difficulty. We found that anterior AC activations were increased during discrimination but not during memory tasks, while activations in the inferior parietal lobule posterior to the AC were enhanced during memory tasks but not during discrimination. We also found that wide areas of the anterior AC and anterior insula were strongly deactivated during the pitch memory tasks. While these results are consistent with the proposition that the anterior and posterior AC belong to functionally separate auditory processing streams, our results show that this division is present also between tasks using spatially invariant sounds. Together, our results indicate that activations of human AC are strongly dependent on the characteristics of the behavioral task.

Brain Science: From the Very Small to the Very Large

We still lack a clear understanding of how brain imaging signals relate to neuronal activity. Recent work shows that the simultaneous activity of neuronal ensembles strongly correlates with local field potentials and imaging measurements.