Maria Chait

Processing Asymmetry of Transitions between Order and Disorder in Human Auditory Cortex

Auditory environments vary as a result of the appearance and disappearance of acoustic sources, as well as fluctuations characteristic of the sources themselves. The appearance of an object is often manifest as a transition in the pattern of ongoing fluctuation, rather than an onset or offset of acoustic power. How does the system detect and process such transitions? Based on magnetoencephalography data, we show that the temporal dynamics and response morphology of the neural temporal-edge detection processes depend in precise ways on the nature of the change. We measure auditory cortical responses to transitions between “disorder,” modeled as a sequence of random frequency tone pips, and “order,” modeled as a constant tone. Such transitions embody key characteristics of natural auditory edges. Early cortical responses (from ∼50 ms post-transition) reveal that order–disorder transitions, and vice versa, are processed by different neural mechanisms. Their dynamics suggest that the auditory cortex optimally adjusts to stimulus statistics, even when this is not required for overt behavior. Furthermore, this response profile bears a striking similarity to that measured from another order–disorder transition, between interaurally correlated and uncorrelated noise, a radically different stimulus. This parallelism suggests the existence of a general mechanism that operates early in the processing stream on the abstract statistics of the auditory input, and is putatively related to the processes of constructing a new representation or detecting a deviation from a previously acquired model of the auditory scene. Together, the data reveal information about the mechanisms with which the brain samples, represents, and detects changes in the environment.

Auditory M50 and M100 responses to broadband noise: functional implications

The functional significance of the M50 and M100 auditory evoked fields remains unclear. Here we report auditory evoked field data from three different studies employing wide-band noise stimuli. We find that, for the same stimuli, the strength of the M100, as well as its lateralization, are task-modulated. The M50, in contrast, shows three properties: It is dramatically more pronounced for noise stimuli than for pure tones, does not seem to be task dependent, and, is significantly stronger in the left hemisphere in all task conditions. These contrasting patterns of activation shed light on the properties of the response-generating mechanisms and suggest roles in the process of auditory figure-ground segregation.

The role of temporal regularity in auditory segregation.

The idea that predictive modelling and extraction of regularities plays a pivotal role in auditory segregation has recently attracted considerable attention. The present study investigated the effect of one basic form of regularity, rhythmic regularity, on auditory stream segregation. We departed from the classic streaming paradigm and developed a new stimulus, Rand-AB, consisting of two, concurrently presented, temporally uncorrelated, tone sequences (with frequencies A and B). To evaluate segregation, we used an objective measure of the extent to which listeners are able to selectively attend to one of the sequences in the presence of the other. Performance was quantified on a difficult pattern detection task which involves detecting a rarely occurring pattern of amplitude modulation applied to three consecutive A or B tones. In all cases the attended sequence was temporally irregular (with a random inter-tone-interval (ITI) between 100 and 400 ms) and the regularity status of the competing sequence was set to one of four conditions: (1) random ITI between 100 and 400 ms (2) isochronous with ITI = 400 ms. (3) isochronous with ITI = 250 ms (equal to the mean rate of the attended sequence) (4) isochronous with ITI = 100 ms. For a frequency separation of 2 (but not 4) semi tones we observed improved performance in conditions (3) and (4) relative to (1), suggesting that stream segregation is facilitated when the distracter sequence is temporally regular, but that the effect of temporal regularity as a cue for segregation is limited to relatively fast rates and to situations where frequency separation is insufficient for segregation. These findings provide new evidence to support models of streaming that involve segregation based on the formation of predictive models.

Brain responses in humans reveal ideal observer-like sensitivity to complex acoustic patterns

Significance We reveal the temporal dynamics and underlying neural sources of the process by which the brain discovers complex temporal patterns in rapidly unfolding sound sequences. We demonstrate that the auditory system, supported by a network of auditory cortical, hippocampal, and frontal sources, continually scans the environment, efficiently represents complex stimulus statistics, and rapidly (close to the bounds implied by an ideal observer model) responds to emergence of regular patterns, even when these are not behaviorally relevant. Neuronal activity correlated with the predictability of ongoing auditory input, both in terms of deterministic structure and the entropy of random sequences, providing clear neurophysiological evidence of the brains capacity to automatically encode high-order statistics in sensory input. We use behavioral methods, magnetoencephalography, and functional MRI to investigate how human listeners discover temporal patterns and statistical regularities in complex sound sequences. Sensitivity to patterns is fundamental to sensory processing, in particular in the auditory system, because most auditory signals only have meaning as successions over time. Previous evidence suggests that the brain is tuned to the statistics of sensory stimulation. However, the process through which this arises has been elusive. We demonstrate that listeners are remarkably sensitive to the emergence of complex patterns within rapidly evolving sound sequences, performing on par with an ideal observer model. Brain responses reveal online processes of evidence accumulation—dynamic changes in tonic activity precisely correlate with the expected precision or predictability of ongoing auditory input—both in terms of deterministic (first-order) structure and the entropy of random sequences. Source analysis demonstrates an interaction between primary auditory cortex, hippocampus, and inferior frontal gyrus in the process of discovering the regularity within the ongoing sound sequence. The results are consistent with precision based predictive coding accounts of perceptual inference and provide compelling neurophysiological evidence of the brains capacity to encode high-order temporal structure in sensory signals.

Auditory temporal edge detection in human auditory cortex

Auditory objects are detected if they differ acoustically from the ongoing background. In simple cases, the appearance or disappearance of an object involves a transition in power, or frequency content, of the ongoing sound. However, it is more realistic that the background and object possess substantial non-stationary statistics, and the task is then to detect a transition in the pattern of ongoing statistics. How does the system detect and process such transitions? We use magnetoencephalography (MEG) to measure early auditory cortical responses to transitions between constant tones, regularly alternating, and randomly alternating tone-pip sequences. Such transitions embody key characteristics of natural auditory temporal edges. Our data demonstrate that the temporal dynamics and response polarity of the neural temporal-edge-detection processes depend in specific ways on the generalized nature of the edge (the context preceding and following the transition) and suggest that distinct neural substrates in core and non-core auditory cortex are recruited depending on the kind of computation (discovery of a violation of regularity, vs. the detection of a new regularity) required to extract the edge from the ongoing fluctuating input entering a listeners ears.

Neural dynamics of attending and ignoring in human auditory cortex

Studies in all sensory modalities have demonstrated amplification of early brain responses to attended signals, but less is known about the processes by which listeners selectively ignore stimuli. Here we use MEG and a new paradigm to dissociate the effects of selectively attending, and ignoring in time. Two different tasks were performed successively on the same acoustic stimuli: triplets of tones (A, B, C) with noise-bursts interspersed between the triplets. In the COMPARE task subjects were instructed to respond when tones A and C were of same frequency. In the PASSIVE task they were instructed to respond as fast as possible to noise-bursts. COMPARE requires attending to A and C and actively ignoring tone B, but PASSIVE involves neither attending to nor ignoring the tones. The data were analyzed separately for frontal and auditory-cortical channels to independently address attentional effects on low-level sensory versus putative control processing. We observe the earliest attend/ignore effects as early as 100 ms post-stimulus onset in auditory cortex. These appear to be generated by modulation of exogenous (stimulus-driven) sensory evoked activity. Specifically related to ignoring, we demonstrate that active-ignoring-induced input inhibition involves early selection. We identified a sequence of early (<200 ms post-onset) auditory cortical effects, comprised of onset response attenuation and the emergence of an inhibitory response, and provide new, direct evidence that listeners actively ignoring a sound can reduce their stimulus related activity in auditory cortex by 100 ms after onset when this is required to execute specific behavioral objectives.

Inattentional Deafness: Visual Load Leads to Time-Specific Suppression of Auditory Evoked Responses

Due to capacity limits on perception, conditions of high perceptual load lead to reduced processing of unattended stimuli (Lavie et al., 2014). Accumulating work demonstrates the effects of visual perceptual load on visual cortex responses, but the effects on auditory processing remain poorly understood. Here we establish the neural mechanisms underlying “inattentional deafness”—the failure to perceive auditory stimuli under high visual perceptual load. Participants performed a visual search task of low (target dissimilar to nontarget items) or high (target similar to nontarget items) load. On a random subset (50%) of trials, irrelevant tones were presented concurrently with the visual stimuli. Brain activity was recorded with magnetoencephalography, and time-locked responses to the visual search array and to the incidental presence of unattended tones were assessed. High, compared to low, perceptual load led to increased early visual evoked responses (within 100 ms from onset). This was accompanied by reduced early (∼100 ms from tone onset) auditory evoked activity in superior temporal sulcus and posterior middle temporal gyrus. A later suppression of the P3 “awareness” response to the tones was also observed under high load. A behavioral experiment revealed reduced tone detection sensitivity under high visual load, indicating that the reduction in neural responses was indeed associated with reduced awareness of the sounds. These findings support a neural account of shared audiovisual resources, which, when depleted under load, leads to failures of sensory perception and awareness. SIGNIFICANCE STATEMENT The present work clarifies the neural underpinning of inattentional deafness under high visual load. The findings of near-simultaneous load effects on both visual and auditory evoked responses suggest shared audiovisual processing capacity. Temporary depletion of shared capacity in perceptually demanding visual tasks leads to a momentary reduction in sensory processing of auditory stimuli, resulting in inattentional deafness. The dynamic “push–pull” pattern of load effects on visual and auditory processing furthers our understanding of both the neural mechanisms of attention and of cross-modal effects across visual and auditory processing. These results also offer an explanation for many previous failures to find cross-modal effects in experiments where the visual load effects may not have coincided directly with auditory sensory processing.

Segregation of complex acoustic scenes based on temporal coherence.

In contrast to the complex acoustic environments we encounter everyday, most studies of auditory segregation have used relatively simple signals. Here, we synthesized a new stimulus to examine the detection of coherent patterns (‘figures’) from overlapping ‘background’ signals. In a series of experiments, we demonstrate that human listeners are remarkably sensitive to the emergence of such figures and can tolerate a variety of spectral and temporal perturbations. This robust behavior is consistent with the existence of automatic auditory segregation mechanisms that are highly sensitive to correlations across frequency and time. The observed behavior cannot be explained purely on the basis of adaptation-based models used to explain the segregation of deterministic narrowband signals. We show that the present results are consistent with the predictions of a model of auditory perceptual organization based on temporal coherence. Our data thus support a role for temporal coherence as an organizational principle underlying auditory segregation. DOI: http://dx.doi.org/10.7554/eLife.00699.001

Is predictability salient? A study of attentional capture by auditory patterns

In this series of behavioural and electroencephalography (EEG) experiments, we investigate the extent to which repeating patterns of sounds capture attention. Work in the visual domain has revealed attentional capture by statistically predictable stimuli, consistent with predictive coding accounts which suggest that attention is drawn to sensory regularities. Here, stimuli comprised rapid sequences of tone pips, arranged in regular (REG) or random (RAND) patterns. EEG data demonstrate that the brain rapidly recognizes predictable patterns manifested as a rapid increase in responses to REG relative to RAND sequences. This increase is reminiscent of the increase in gain on neural responses to attended stimuli often seen in the neuroimaging literature, and thus consistent with the hypothesis that predictable sequences draw attention. To study potential attentional capture by auditory regularities, we used REG and RAND sequences in two different behavioural tasks designed to reveal effects of attentional capture by regularity. Overall, the pattern of results suggests that regularity does not capture attention. This article is part of the themed issue ‘Auditory and visual scene analysis’.

Delayed Detection of Tonal Targets in Background Noise in Dyslexia.

Individuals with developmental dyslexia are often impaired in their ability to process certain linguistic and even basic non-linguistic auditory signals. Recent investigations report conflicting findings regarding impaired low-level binaural detection mechanisms associated with dyslexia. Binaural impairment has been hypothesized to stem from a general low-level processing disorder for temporally fine sensory stimuli. Here we use a new behavioral paradigm to address this issue. We compared the response times of dyslexic listeners and their matched controls in a tone-in-noise detection task. The tonal signals were either Huggins Pitch (HP), a stimulus requiring binaural processing to elicit a pitch percept, or a pure tone-perceptually similar but physically very different signals. The results showed no difference between the two groups specific to the processing of HP and thus no evidence for a binaural impairment in dyslexia. However, dyslexic subjects exhibited a general difficulty in extracting tonal objects from background noise, manifested by a globally delayed detection speed.