Models optimized for real-world tasks reveal the necessity of precise temporal coding in hearing.

Neurons encode information in the timing of their spikes in addition to their firing rates. Spike timing is particularly precise in the auditory nerve, where action potentials phase lock to sound with sub-millisecond precision, but its behavioral relevance is uncertain. To investigate the role of this temporal coding, we optimized machine learning models to perform real-world hearing tasks with simulated cochlear input. We asked how precise auditory nerve spike timing needed to be to reproduce human behavior. Models with high-fidelity phase locking exhibited more human-like sound localization and speech perception than models without, consistent with an essential role in human hearing. Degrading phase locking produced task-dependent effects, revealing how the use of fine-grained temporal information reflects both ecological task demands and neural implementation constraints. The results link neural coding to perception and clarify conditions in which prostheses that fail to restore high-fidelity temporal coding could in principle restore near-normal hearing.

Commonality and variation in mental representations of music revealed by a cross-cultural comparison of rhythm priors in 15 countries.

Music is present in every known society but varies from place to place. What, if anything, is universal to music cognition? We measured a signature of mental representations of rhythm in 39 participant groups in 15 countries, spanning urban societies and Indigenous populations. Listeners reproduced random 'seed' rhythms; their reproductions were fed back as the stimulus (as in the game of 'telephone'), such that their biases (the prior) could be estimated from the distribution of reproductions. Every tested group showed a sparse prior with peaks at integer-ratio rhythms. However, the importance of different integer ratios varied across groups, often reflecting local musical practices. Our results suggest a common feature of music cognition: discrete rhythm 'categories' at small-integer ratios. These discrete representations plausibly stabilize musical systems in the face of cultural transmission but interact with culture-specific traditions to yield the diversity that is evident when mental representations are probed across many cultures.

Many but not all deep neural network audio models capture brain responses and exhibit correspondence between model stages and brain regions.

Models that predict brain responses to stimuli provide one measure of understanding of a sensory system and have many potential applications in science and engineering. Deep artificial neural networks have emerged as the leading such predictive models of the visual system but are less explored in audition. Prior work provided examples of audio-trained neural networks that produced good predictions of auditory cortical fMRI responses and exhibited correspondence between model stages and brain regions, but left it unclear whether these results generalize to other neural network models and, thus, how to further improve models in this domain. We evaluated model-brain correspondence for publicly available audio neural network models along with in-house models trained on 4 different tasks. Most tested models outpredicted standard spectromporal filter-bank models of auditory cortex and exhibited systematic model-brain correspondence: Middle stages best predicted primary auditory cortex, while deep stages best predicted non-primary cortex. However, some state-of-the-art models produced substantially worse brain predictions. Models trained to recognize speech in background noise produced better brain predictions than models trained to recognize speech in quiet, potentially because hearing in noise imposes constraints on biological auditory representations. The training task influenced the prediction quality for specific cortical tuning properties, with best overall predictions resulting from models trained on multiple tasks. The results generally support the promise of deep neural networks as models of audition, though they also indicate that current models do not explain auditory cortical responses in their entirety.

Model metamers reveal divergent invariances between biological and artificial neural networks.

Deep neural network models of sensory systems are often proposed to learn representational transformations with invariances like those in the brain. To reveal these invariances, we generated 'model metamers', stimuli whose activations within a model stage are matched to those of a natural stimulus. Metamers for state-of-the-art supervised and unsupervised neural network models of vision and audition were often completely unrecognizable to humans when generated from late model stages, suggesting differences between model and human invariances. Targeted model changes improved human recognizability of model metamers but did not eliminate the overall human-model discrepancy. The human recognizability of a model's metamers was well predicted by their recognizability by other models, suggesting that models contain idiosyncratic invariances in addition to those required by the task. Metamer recognizability dissociated from both traditional brain-based benchmarks and adversarial vulnerability, revealing a distinct failure mode of existing sensory models and providing a complementary benchmark for model assessment.

Relative pitch representations and invariance to timbre.

Information in speech and music is often conveyed through changes in fundamental frequency (f0), perceived by humans as "relative pitch". Relative pitch judgments are complicated by two facts. First, sounds can simultaneously vary in timbre due to filtering imposed by a vocal tract or instrument body. Second, relative pitch can be extracted in two ways: by measuring changes in constituent frequency components from one sound to another, or by estimating the f0 of each sound and comparing the estimates. We examined the effects of timbral differences on relative pitch judgments, and whether any invariance to timbre depends on whether judgments are based on constituent frequencies or their f0. Listeners performed up/down and interval discrimination tasks with pairs of spoken vowels, instrument notes, or synthetic tones, synthesized to be either harmonic or inharmonic. Inharmonic sounds lack a well-defined f0, such that relative pitch must be extracted from changes in individual frequencies. Pitch judgments were less accurate when vowels/instruments were different compared to when they were the same, and were biased by the associated timbre differences. However, this bias was similar for harmonic and inharmonic sounds, and was observed even in conditions where judgments of harmonic sounds were based on f0 representations. Relative pitch judgments are thus not invariant to timbre, even when timbral variation is naturalistic, and when such judgments are based on representations of f0.

Harmonicity aids hearing in noise.

Hearing in noise is a core problem in audition, and a challenge for hearing-impaired listeners, yet the underlying mechanisms are poorly understood. We explored whether harmonic frequency relations, a signature property of many communication sounds, aid hearing in noise for normal hearing listeners. We measured detection thresholds in noise for tones and speech synthesized to have harmonic or inharmonic spectra. Harmonic signals were consistently easier to detect than otherwise identical inharmonic signals. Harmonicity also improved discrimination of sounds in noise. The largest benefits were observed for two-note up-down "pitch" discrimination and melodic contour discrimination, both of which could be performed equally well with harmonic and inharmonic tones in quiet, but which showed large harmonic advantages in noise. The results show that harmonicity facilitates hearing in noise, plausibly by providing a noise-robust pitch cue that aids detection and discrimination.

A neural population selective for song in human auditory cortex.

How is music represented in the brain? While neuroimaging has revealed some spatial segregation between responses to music versus other sounds, little is known about the neural code for music itself. To address this question, we developed a method to infer canonical response components of human auditory cortex using intracranial responses to natural sounds, and further used the superior coverage of fMRI to map their spatial distribution. The inferred components replicated many prior findings, including distinct neural selectivity for speech and music, but also revealed a novel component that responded nearly exclusively to music with singing. Song selectivity was not explainable by standard acoustic features, was located near speech- and music-selective responses, and was also evident in individual electrodes. These results suggest that representations of music are fractionated into subpopulations selective for different types of music, one of which is specialized for the analysis of song.

Deep neural network models of sound localization reveal how perception is adapted to real-world environments.

Mammals localize sounds using information from their two ears. Localization in real-world conditions is challenging, as echoes provide erroneous information and noises mask parts of target sounds. To better understand real-world localization, we equipped a deep neural network with human ears and trained it to localize sounds in a virtual environment. The resulting model localized accurately in realistic conditions with noise and reverberation. In simulated experiments, the model exhibited many features of human spatial hearing: sensitivity to monaural spectral cues and interaural time and level differences, integration across frequency, biases for sound onsets and limits on localization of concurrent sources. But when trained in unnatural environments without reverberation, noise or natural sounds, these performance characteristics deviated from those of humans. The results show how biological hearing is adapted to the challenges of real-world environments and illustrate how artificial neural networks can reveal the real-world constraints that shape perception.

Deep neural network models reveal interplay of peripheral coding and stimulus statistics in pitch perception.

Perception is thought to be shaped by the environments for which organisms are optimized. These influences are difficult to test in biological organisms but may be revealed by machine perceptual systems optimized under different conditions. We investigated environmental and physiological influences on pitch perception, whose properties are commonly linked to peripheral neural coding limits. We first trained artificial neural networks to estimate fundamental frequency from biologically faithful cochlear representations of natural sounds. The best-performing networks replicated many characteristics of human pitch judgments. To probe the origins of these characteristics, we then optimized networks given altered cochleae or sound statistics. Human-like behavior emerged only when cochleae had high temporal fidelity and when models were optimized for naturalistic sounds. The results suggest pitch perception is critically shaped by the constraints of natural environments in addition to those of the cochlea, illustrating the use of artificial neural networks to reveal underpinnings of behavior.

Causal inference in environmental sound recognition.

Sound is caused by physical events in the world. Do humans infer these causes when recognizing sound sources? We tested whether the recognition of common environmental sounds depends on the inference of a basic physical variable - the source intensity (i.e., the power that produces a sound). A source's intensity can be inferred from the intensity it produces at the ear and its distance, which is normally conveyed by reverberation. Listeners could thus use intensity at the ear and reverberation to constrain recognition by inferring the underlying source intensity. Alternatively, listeners might separate these acoustic cues from their representation of a sound's identity in the interest of invariant recognition. We compared these two hypotheses by measuring recognition accuracy for sounds with typically low or high source intensity (e.g., pepper grinders vs. trucks) that were presented across a range of intensities at the ear or with reverberation cues to distance. The recognition of low-intensity sources (e.g., pepper grinders) was impaired by high presentation intensities or reverberation that conveyed distance, either of which imply high source intensity. Neither effect occurred for high-intensity sources. The results suggest that listeners implicitly use the intensity at the ear along with distance cues to infer a source's power and constrain its identity. The recognition of real-world sounds thus appears to depend upon the inference of their physical generative parameters, even generative parameters whose cues might otherwise be separated from the representation of a sound's identity.

Music-selective neural populations arise without musical training.

Recent work has shown that human auditory cortex contains neural populations anterior and posterior to primary auditory cortex that respond selectively to music. However, it is unknown how this selectivity for music arises. To test whether musical training is necessary, we measured fMRI responses to 192 natural sounds in 10 people with almost no musical training. When voxel responses were decomposed into underlying components, this group exhibited a music-selective component that was very similar in response profile and anatomical distribution to that previously seen in individuals with moderate musical training. We also found that musical genres that were less familiar to our participants (e.g., Balinese gamelan) produced strong responses within the music component, as did drum clips with rhythm but little melody, suggesting that these neural populations are broadly responsive to music as a whole. Our findings demonstrate that the signature properties of neural music selectivity do not require musical training to develop, showing that the music-selective neural populations are a fundamental and widespread property of the human brain.NEW & NOTEWORTHY We show that music-selective neural populations are clearly present in people without musical training, demonstrating that they are a fundamental and widespread property of the human brain. Additionally, we show music-selective neural populations respond strongly to music from unfamiliar genres as well as music with rhythm but little pitch information, suggesting that they are broadly responsive to music as a whole.

Time-dependent discrimination advantages for harmonic sounds suggest efficient coding for memory.

Perceptual systems have finite memory resources and must store incoming signals in compressed formats. To explore whether representations of a sound's pitch might derive from this need for compression, we compared discrimination of harmonic and inharmonic sounds across delays. In contrast to inharmonic spectra, harmonic spectra can be summarized, and thus compressed, using their fundamental frequency (f0). Participants heard two sounds and judged which was higher. Despite being comparable for sounds presented back-to-back, discrimination was better for harmonic than inharmonic stimuli when sounds were separated in time, implicating memory representations unique to harmonic sounds. Patterns of individual differences (correlations between thresholds in different conditions) indicated that listeners use different representations depending on the time delay between sounds, directly comparing the spectra of temporally adjacent sounds, but transitioning to comparing f0s across delays. The need to store sound in memory appears to determine reliance on f0-based pitch and may explain its importance in music, in which listeners must extract relationships between notes separated in time.

Perceptual fusion of musical notes by native Amazonians suggests universal representations of musical intervals.

Music perception is plausibly constrained by universal perceptual mechanisms adapted to natural sounds. Such constraints could arise from our dependence on harmonic frequency spectra for segregating concurrent sounds, but evidence has been circumstantial. We measured the extent to which concurrent musical notes are misperceived as a single sound, testing Westerners as well as native Amazonians with limited exposure to Western music. Both groups were more likely to mistake note combinations related by simple integer ratios as single sounds ('fusion'). Thus, even with little exposure to Western harmony, acoustic constraints on sound segregation appear to induce perceptual structure on note combinations. However, fusion did not predict aesthetic judgments of intervals in Westerners, or in Amazonians, who were indifferent to consonance/dissonance. The results suggest universal perceptual mechanisms that could help explain cross-cultural regularities in musical systems, but indicate that these mechanisms interact with culture-specific influences to produce musical phenomena such as consonance.

Development of consonance preferences in Western listeners.

Many scholars consider preferences for consonance, as defined by Western music theorists, to be based primarily on biological factors, while others emphasize experiential factors, notably the nature of musical exposure. Cross-cultural experiments suggest that consonance preferences are shaped by musical experience, implying that preferences should emerge or become stronger over development for individuals in Western cultures. However, little is known about this developmental trajectory. We measured preferences for the consonance of simultaneous sounds and related acoustic properties in children and adults to characterize their developmental course and dependence on musical experience. In Study 1, adults and children 6 to 10 years of age rated their liking of simultaneous tone combinations (dyads) and affective vocalizations. Preferences for consonance increased with age and were predicted by changing preferences for harmonicity-the degree to which a sound's frequencies are multiples of a common fundamental frequency-but not by evaluations of beating-fluctuations in amplitude that occur when frequencies are close but not identical, producing the sensation of acoustic roughness. In Study 2, musically trained adults and 10-year-old children also rated the same stimuli. Age and musical training were associated with enhanced preference for consonance. Both measures of experience were associated with an enhanced preference for harmonicity, but were unrelated to evaluations of beating stimuli. The findings are consistent with cross-cultural evidence and the effects of musicianship in Western adults in linking Western musical experience to preferences for consonance and harmonicity. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Ecological origins of perceptual grouping principles in the auditory system.

Events and objects in the world must be inferred from sensory signals to support behavior. Because sensory measurements are temporally and spatially local, the estimation of an object or event can be viewed as the grouping of these measurements into representations of their common causes. Perceptual grouping is believed to reflect internalized regularities of the natural environment, yet grouping cues have traditionally been identified using informal observation and investigated using artificial stimuli. The relationship of grouping to natural signal statistics has thus remained unclear, and additional or alternative cues remain possible. Here, we develop a general methodology for relating grouping to natural sensory signals and apply it to derive auditory grouping cues from natural sounds. We first learned local spectrotemporal features from natural sounds and measured their co-occurrence statistics. We then learned a small set of stimulus properties that could predict the measured feature co-occurrences. The resulting cues included established grouping cues, such as harmonic frequency relationships and temporal coincidence, but also revealed previously unappreciated grouping principles. Human perceptual grouping was predicted by natural feature co-occurrence, with humans relying on the derived grouping cues in proportion to their informativity about co-occurrence in natural sounds. The results suggest that auditory grouping is adapted to natural stimulus statistics, show how these statistics can reveal previously unappreciated grouping phenomena, and provide a framework for studying grouping in natural signals.

Illusory sound texture reveals multi-second statistical completion in auditory scene analysis.

Sound sources in the world are experienced as stable even when intermittently obscured, implying perceptual completion mechanisms that "fill in" missing sensory information. We demonstrate a filling-in phenomenon in which the brain extrapolates the statistics of background sounds (textures) over periods of several seconds when they are interrupted by another sound, producing vivid percepts of illusory texture. The effect differs from previously described completion effects in that 1) the extrapolated sound must be defined statistically given the stochastic nature of texture, and 2) the effect lasts much longer, enabling introspection and facilitating assessment of the underlying representation. Illusory texture biases subsequent texture statistic estimates indistinguishably from actual texture, suggesting that it is represented similarly to actual texture. The illusion appears to represent an inference about whether the background is likely to continue during concurrent sounds, providing a stable statistical representation of the ongoing environment despite unstable sensory evidence.

Universal and Non-universal Features of Musical Pitch Perception Revealed by Singing.

Musical pitch perception is argued to result from nonmusical biological constraints and thus to have similar characteristics across cultures, but its universality remains unclear. We probed pitch representations in residents of the Bolivian Amazon-the Tsimane', who live in relative isolation from Western culture-as well as US musicians and non-musicians. Participants sang back tone sequences presented in different frequency ranges. Sung responses of Amazonian and US participants approximately replicated heard intervals on a logarithmic scale, even for tones outside the singing range. Moreover, Amazonian and US reproductions both deteriorated for high-frequency tones even though they were fully audible. But whereas US participants tended to reproduce notes an integer number of octaves above or below the heard tones, Amazonians did not, ignoring the note "chroma" (C, D, etc.). Chroma matching in US participants was more pronounced in US musicians than non-musicians, was not affected by feedback, and was correlated with similarity-based measures of octave equivalence as well as the ability to match the absolute f0 of a stimulus in the singing range. The results suggest the cross-cultural presence of logarithmic scales for pitch, and biological constraints on the limits of pitch, but indicate that octave equivalence may be culturally contingent, plausibly dependent on pitch representations that develop from experience with particular musical systems. VIDEO ABSTRACT.

Invariance to background noise as a signature of non-primary auditory cortex.

Despite well-established anatomical differences between primary and non-primary auditory cortex, the associated representational transformations have remained elusive. Here we show that primary and non-primary auditory cortex are differentiated by their invariance to real-world background noise. We measured fMRI responses to natural sounds presented in isolation and in real-world noise, quantifying invariance as the correlation between the two responses for individual voxels. Non-primary areas were substantially more noise-invariant than primary areas. This primary-nonprimary difference occurred both for speech and non-speech sounds and was unaffected by a concurrent demanding visual task, suggesting that the observed invariance is not specific to speech processing and is robust to inattention. The difference was most pronounced for real-world background noise-both primary and non-primary areas were relatively robust to simple types of synthetic noise. Our results suggest a general representational transformation between auditory cortical stages, illustrating a representational consequence of hierarchical organization in the auditory system.