Large-scale single-neuron speech sound encoding across the depth of human cortex.

Understanding the neural basis of speech perception requires that we study the human brain both at the scale of the fundamental computational unit of neurons and in their organization across the depth of cortex. Here we used high-density Neuropixels arrays1-3 to record from 685 neurons across cortical layers at nine sites in a high-level auditory region that is critical for speech, the superior temporal gyrus4,5, while participants listened to spoken sentences. Single neurons encoded a wide range of speech sound cues, including features of consonants and vowels, relative vocal pitch, onsets, amplitude envelope and sequence statistics. Neurons at each cross-laminar recording exhibited dominant tuning to a primary speech feature while also containing a substantial proportion of neurons that encoded other features contributing to heterogeneous selectivity. Spatially, neurons at similar cortical depths tended to encode similar speech features. Activity across all cortical layers was predictive of high-frequency field potentials (electrocorticography), providing a neuronal origin for macroelectrode recordings from the cortical surface. Together, these results establish single-neuron tuning across the cortical laminae as an important dimension of speech encoding in human superior temporal gyrus.

Single-neuronal elements of speech production in humans.

Humans are capable of generating extraordinarily diverse articulatory movement combinations to produce meaningful speech. This ability to orchestrate specific phonetic sequences, and their syllabification and inflection over subsecond timescales allows us to produce thousands of word sounds and is a core component of language1,2. The fundamental cellular units and constructs by which we plan and produce words during speech, however, remain largely unknown. Here, using acute ultrahigh-density Neuropixels recordings capable of sampling across the cortical column in humans, we discover neurons in the language-dominant prefrontal cortex that encoded detailed information about the phonetic arrangement and composition of planned words during the production of natural speech. These neurons represented the specific order and structure of articulatory events before utterance and reflected the segmentation of phonetic sequences into distinct syllables. They also accurately predicted the phonetic, syllabic and morphological components of upcoming words and showed a temporally ordered dynamic. Collectively, we show how these mixtures of cells are broadly organized along the cortical column and how their activity patterns transition from articulation planning to production. We also demonstrate how these cells reliably track the detailed composition of consonant and vowel sounds during perception and how they distinguish processes specifically related to speaking from those related to listening. Together, these findings reveal a remarkably structured organization and encoding cascade of phonetic representations by prefrontal neurons in humans and demonstrate a cellular process that can support the production of speech.

A tribute to a remarkably sound solution.

For their work on the development of the modern cochlear implant, which bestows hearing to individuals with profound deafness, Ingeborg Hochmair, Graeme Clark, and Blake Wilson are the 2013 recipients of the Lasker∼DeBakey Clinical Medical Research Award.

Original speech and its echo are segregated and separately processed in the human brain.

Speech recognition crucially relies on slow temporal modulations (<16 Hz) in speech. Recent studies, however, have demonstrated that the long-delay echoes, which are common during online conferencing, can eliminate crucial temporal modulations in speech but do not affect speech intelligibility. Here, we investigated the underlying neural mechanisms. MEG experiments demonstrated that cortical activity can effectively track the temporal modulations eliminated by an echo, which cannot be fully explained by basic neural adaptation mechanisms. Furthermore, cortical responses to echoic speech can be better explained by a model that segregates speech from its echo than by a model that encodes echoic speech as a whole. The speech segregation effect was observed even when attention was diverted but would disappear when segregation cues, i.e., speech fine structure, were removed. These results strongly suggested that, through mechanisms such as stream segregation, the auditory system can build an echo-insensitive representation of speech envelope, which can support reliable speech recognition.

Attention to audiovisual speech shapes neural processing through feedback-feedforward loops between different nodes of the speech network.

Selective attention-related top-down modulation plays a significant role in separating relevant speech from irrelevant background speech when vocal attributes separating concurrent speakers are small and continuously evolving. Electrophysiological studies have shown that such top-down modulation enhances neural tracking of attended speech. Yet, the specific cortical regions involved remain unclear due to the limited spatial resolution of most electrophysiological techniques. To overcome such limitations, we collected both electroencephalography (EEG) (high temporal resolution) and functional magnetic resonance imaging (fMRI) (high spatial resolution), while human participants selectively attended to speakers in audiovisual scenes containing overlapping cocktail party speech. To utilise the advantages of the respective techniques, we analysed neural tracking of speech using the EEG data and performed representational dissimilarity-based EEG-fMRI fusion. We observed that attention enhanced neural tracking and modulated EEG correlates throughout the latencies studied. Further, attention-related enhancement of neural tracking fluctuated in predictable temporal profiles. We discuss how such temporal dynamics could arise from a combination of interactions between attention and prediction as well as plastic properties of the auditory cortex. EEG-fMRI fusion revealed attention-related iterative feedforward-feedback loops between hierarchically organised nodes of the ventral auditory object related processing stream. Our findings support models where attention facilitates dynamic neural changes in the auditory cortex, ultimately aiding discrimination of relevant sounds from irrelevant ones while conserving neural resources.

The human auditory system uses amplitude modulation to distinguish music from speech.

Music and speech are complex and distinct auditory signals that are both foundational to the human experience. The mechanisms underpinning each domain are widely investigated. However, what perceptual mechanism transforms a sound into music or speech and how basic acoustic information is required to distinguish between them remain open questions. Here, we hypothesized that a sound's amplitude modulation (AM), an essential temporal acoustic feature driving the auditory system across processing levels, is critical for distinguishing music and speech. Specifically, in contrast to paradigms using naturalistic acoustic signals (that can be challenging to interpret), we used a noise-probing approach to untangle the auditory mechanism: If AM rate and regularity are critical for perceptually distinguishing music and speech, judging artificially noise-synthesized ambiguous audio signals should align with their AM parameters. Across 4 experiments (N = 335), signals with a higher peak AM frequency tend to be judged as speech, lower as music. Interestingly, this principle is consistently used by all listeners for speech judgments, but only by musically sophisticated listeners for music. In addition, signals with more regular AM are judged as music over speech, and this feature is more critical for music judgment, regardless of musical sophistication. The data suggest that the auditory system can rely on a low-level acoustic property as basic as AM to distinguish music from speech, a simple principle that provokes both neurophysiological and evolutionary experiments and speculations.

Phase-dependent word perception emerges from region-specific sensitivity to the statistics of language.

Neural oscillations reflect fluctuations in excitability, which biases the percept of ambiguous sensory input. Why this bias occurs is still not fully understood. We hypothesized that neural populations representing likely events are more sensitive, and thereby become active on earlier oscillatory phases, when the ensemble itself is less excitable. Perception of ambiguous input presented during less-excitable phases should therefore be biased toward frequent or predictable stimuli that have lower activation thresholds. Here, we show such a frequency bias in spoken word recognition using psychophysics, magnetoencephalography (MEG), and computational modelling. With MEG, we found a double dissociation, where the phase of oscillations in the superior temporal gyrus and medial temporal gyrus biased word-identification behavior based on phoneme and lexical frequencies, respectively. This finding was reproduced in a computational model. These results demonstrate that oscillations provide a temporal ordering of neural activity based on the sensitivity of separable neural populations.

Distinct neural encoding of glimpsed and masked speech in multitalker situations.

Humans can easily tune in to one talker in a multitalker environment while still picking up bits of background speech; however, it remains unclear how we perceive speech that is masked and to what degree non-target speech is processed. Some models suggest that perception can be achieved through glimpses, which are spectrotemporal regions where a talker has more energy than the background. Other models, however, require the recovery of the masked regions. To clarify this issue, we directly recorded from primary and non-primary auditory cortex (AC) in neurosurgical patients as they attended to one talker in multitalker speech and trained temporal response function models to predict high-gamma neural activity from glimpsed and masked stimulus features. We found that glimpsed speech is encoded at the level of phonetic features for target and non-target talkers, with enhanced encoding of target speech in non-primary AC. In contrast, encoding of masked phonetic features was found only for the target, with a greater response latency and distinct anatomical organization compared to glimpsed phonetic features. These findings suggest separate mechanisms for encoding glimpsed and masked speech and provide neural evidence for the glimpsing model of speech perception.

A deep hierarchy of predictions enables online meaning extraction in a computational model of human speech comprehension.

Understanding speech requires mapping fleeting and often ambiguous soundwaves to meaning. While humans are known to exploit their capacity to contextualize to facilitate this process, how internal knowledge is deployed online remains an open question. Here, we present a model that extracts multiple levels of information from continuous speech online. The model applies linguistic and nonlinguistic knowledge to speech processing, by periodically generating top-down predictions and incorporating bottom-up incoming evidence in a nested temporal hierarchy. We show that a nonlinguistic context level provides semantic predictions informed by sensory inputs, which are crucial for disambiguating among multiple meanings of the same word. The explicit knowledge hierarchy of the model enables a more holistic account of the neurophysiological responses to speech compared to using lexical predictions generated by a neural network language model (GPT-2). We also show that hierarchical predictions reduce peripheral processing via minimizing uncertainty and prediction error. With this proof-of-concept model, we demonstrate that the deployment of hierarchical predictions is a possible strategy for the brain to dynamically utilize structured knowledge and make sense of the speech input.

A minimal physics-based model for musical perception.

Some people, entirely untrained in music, can listen to a song and replicate it on a piano with unnerving accuracy. What enables some to "hear" music so much better than others? Long-standing research confirms that part of the answer is undoubtedly neurological and can be improved with training. However, are there structural, physical, or engineering attributes of the human hearing mechanism apparatus (i.e., the hair cells of the internal ear) that render one human innately superior to another in terms of propensity to listen to music? In this work, we investigate a physics-based model of the electromechanics of the hair cells in the inner ear to understand why a person might be physiologically better poised to distinguish musical sounds. A key feature of the model is that we avoid a "black-box" systems-type approach. All parameters are well-defined physical quantities, including membrane thickness, bending modulus, electromechanical properties, and geometrical features, among others. Using the two-tone interference problem as a proxy for musical perception, our model allows us to establish the basis for exploring the effect of external factors such as medicine or environment. As an example of the insights we obtain, we conclude that the reduction in bending modulus of the cell membranes (which for instance may be caused by the usage of a certain class of analgesic drugs) or an increase in the flexoelectricity of the hair cell membrane can interfere with the perception of two-tone excitation.

Do some languages sound more beautiful than others?

Italian is sexy, German is rough-but how about Páez or Tamil? Are there universal phonesthetic judgments based purely on the sound of a language, or are preferences attributable to language-external factors such as familiarity and cultural stereotypes? We collected 2,125 recordings of 228 languages from 43 language families, including 5 to 11 speakers of each language to control for personal vocal attractiveness, and asked 820 native speakers of English, Chinese, or Semitic languages to indicate how much they liked these languages. We found a strong preference for languages perceived as familiar, even when they were misidentified, a variety of cultural-geographical biases, and a preference for breathy female voices. The scores by English, Chinese, and Semitic speakers were weakly correlated, indicating some cross-cultural concordance in phonesthetic judgments, but overall there was little consensus between raters about which languages sounded more beautiful, and average scores per language remained within ±2% after accounting for confounds related to familiarity and voice quality of individual speakers. None of the tested phonetic features-the presence of specific phonemic classes, the overall size of phonetic repertoire, its typicality and similarity to the listener's first language-were robust predictors of pleasantness ratings, apart from a possible slight preference for nontonal languages. While population-level phonesthetic preferences may exist, their contribution to perceptual judgments of short speech recordings appears to be minor compared to purely personal preferences, the speaker's voice quality, and perceived resemblance to other languages culturally branded as beautiful or ugly.

Neural tracking measures of speech intelligibility: Manipulating intelligibility while keeping acoustics unchanged.

Neural speech tracking has advanced our understanding of how our brains rapidly map an acoustic speech signal onto linguistic representations and ultimately meaning. It remains unclear, however, how speech intelligibility is related to the corresponding neural responses. Many studies addressing this question vary the level of intelligibility by manipulating the acoustic waveform, but this makes it difficult to cleanly disentangle the effects of intelligibility from underlying acoustical confounds. Here, using magnetoencephalography recordings, we study neural measures of speech intelligibility by manipulating intelligibility while keeping the acoustics strictly unchanged. Acoustically identical degraded speech stimuli (three-band noise-vocoded, ~20 s duration) are presented twice, but the second presentation is preceded by the original (nondegraded) version of the speech. This intermediate priming, which generates a "pop-out" percept, substantially improves the intelligibility of the second degraded speech passage. We investigate how intelligibility and acoustical structure affect acoustic and linguistic neural representations using multivariate temporal response functions (mTRFs). As expected, behavioral results confirm that perceived speech clarity is improved by priming. mTRFs analysis reveals that auditory (speech envelope and envelope onset) neural representations are not affected by priming but only by the acoustics of the stimuli (bottom-up driven). Critically, our findings suggest that segmentation of sounds into words emerges with better speech intelligibility, and most strongly at the later (~400 ms latency) word processing stage, in prefrontal cortex, in line with engagement of top-down mechanisms associated with priming. Taken together, our results show that word representations may provide some objective measures of speech comprehension.

Perceptual specializations for processing species-specific vocalizations in the common marmoset (Callithrix jacchus).

How humans and animals segregate sensory information into discrete, behaviorally meaningful categories is one of the hallmark questions in neuroscience. Much of the research around this topic in the auditory system has centered around human speech perception, in which categorical processes result in an enhanced sensitivity for acoustically meaningful differences and a reduced sensitivity for nonmeaningful distinctions. Much less is known about whether nonhuman primates process their species-specific vocalizations in a similar manner. We address this question in the common marmoset, a small arboreal New World primate with a rich vocal repertoire produced across a range of behavioral contexts. We first show that marmosets perceptually categorize their vocalizations in ways that correspond to previously defined call types for this species. Next, we show that marmosets are differentially sensitive to changes in particular acoustic features of their most common call types and that these sensitivity differences are matched to the population statistics of their vocalizations in ways that likely maximize category formation. Finally, we show that marmosets are less sensitive to changes in these acoustic features when within the natural range of variability of their calls, which possibly reflects perceptual specializations which maintain existing call categories. These findings suggest specializations for categorical vocal perception in a New World primate species and pave the way for future studies examining their underlying neural mechanisms.

Neural representations of the content and production of human vocalization.

Speech, as the spoken form of language, is fundamental for human communication. The phenomenon of covert inner speech implies functional independence of speech content and motor production. However, it remains unclear how a flexible mapping between speech content and production is achieved on the neural level. To address this, we recorded magnetoencephalography in humans performing a rule-based vocalization task. On each trial, vocalization content (one of two vowels) and production form (overt or covert) were instructed independently. Using multivariate pattern analysis, we found robust neural information about vocalization content and production, mostly originating from speech areas of the left hemisphere. Production signals dynamically transformed upon presentation of the content cue, whereas content signals remained largely stable throughout the trial. In sum, our results show dissociable neural representations of vocalization content and production in the human brain and provide insights into the neural dynamics underlying human vocalization.

Neural Representations of Non-native Speech Reflect Proficiency and Interference from Native Language Knowledge.

Learning to process speech in a foreign language involves learning new representations for mapping the auditory signal to linguistic structure. Behavioral experiments suggest that even listeners that are highly proficient in a non-native language experience interference from representations of their native language. However, much of the evidence for such interference comes from tasks that may inadvertently increase the salience of native language competitors. Here we tested for neural evidence of proficiency and native language interference in a naturalistic story listening task. We studied electroencephalography responses of 39 native speakers of Dutch (14 male) to an English short story, spoken by a native speaker of either American English or Dutch. We modeled brain responses with multivariate temporal response functions, using acoustic and language models. We found evidence for activation of Dutch language statistics when listening to English, but only when it was spoken with a Dutch accent. This suggests that a naturalistic, monolingual setting decreases the interference from native language representations, whereas an accent in the listener's own native language may increase native language interference, by increasing the salience of the native language and activating native language phonetic and lexical representations. Brain responses suggest that such interference stems from words from the native language competing with the foreign language in a single word recognition system, rather than being activated in a parallel lexicon. We further found that secondary acoustic representations of speech (after 200 ms latency) decreased with increasing proficiency. This may reflect improved acoustic-phonetic models in more proficient listeners.Significance Statement Behavioral experiments suggest that native language knowledge interferes with foreign language listening, but such effects may be sensitive to task manipulations, as tasks that increase metalinguistic awareness may also increase native language interference. This highlights the need for studying non-native speech processing using naturalistic tasks. We measured neural responses unobtrusively while participants listened for comprehension and characterized the influence of proficiency at multiple levels of representation. We found that salience of the native language, as manipulated through speaker accent, affected activation of native language representations: significant evidence for activation of native language (Dutch) categories was only obtained when the speaker had a Dutch accent, whereas no significant interference was found to a speaker with a native (American) accent.

Attention Drives Visual Processing and Audiovisual Integration During Multimodal Communication.

During communication in real-life settings, our brain often needs to integrate auditory and visual information and at the same time actively focus on the relevant sources of information, while ignoring interference from irrelevant events. The interaction between integration and attention processes remains poorly understood. Here, we use rapid invisible frequency tagging and magnetoencephalography to investigate how attention affects auditory and visual information processing and integration, during multimodal communication. We presented human participants (male and female) with videos of an actress uttering action verbs (auditory; tagged at 58 Hz) accompanied by two movie clips of hand gestures on both sides of fixation (attended stimulus tagged at 65 Hz; unattended stimulus tagged at 63 Hz). Integration difficulty was manipulated by a lower-order auditory factor (clear/degraded speech) and a higher-order visual semantic factor (matching/mismatching gesture). We observed an enhanced neural response to the attended visual information during degraded speech compared to clear speech. For the unattended information, the neural response to mismatching gestures was enhanced compared to matching gestures. Furthermore, signal power at the intermodulation frequencies of the frequency tags, indexing nonlinear signal interactions, was enhanced in the left frontotemporal and frontal regions. Focusing on the left inferior frontal gyrus, this enhancement was specific for the attended information, for those trials that benefitted from integration with a matching gesture. Together, our results suggest that attention modulates audiovisual processing and interaction, depending on the congruence and quality of the sensory input.

Speech Prosody Serves Temporal Prediction of Language via Contextual Entrainment.

Temporal prediction assists language comprehension. In a series of recent behavioral studies, we have shown that listeners specifically employ rhythmic modulations of prosody to estimate the duration of upcoming sentences, thereby speeding up comprehension. In the current human magnetoencephalography (MEG) study on participants of either sex, we show that the human brain achieves this function through a mechanism termed entrainment. Through entrainment, electrophysiological brain activity maintains and continues contextual rhythms beyond their offset. Our experiment combined exposure to repetitive prosodic contours with the subsequent presentation of visual sentences that either matched or mismatched the duration of the preceding contour. During exposure to prosodic contours, we observed MEG coherence with the contours, which was source-localized to right-hemispheric auditory areas. During the processing of the visual targets, activity at the frequency of the preceding contour was still detectable in the MEG; yet sources shifted to the (left) frontal cortex, in line with a functional inheritance of the rhythmic acoustic context for prediction. Strikingly, when the target sentence was shorter than expected from the preceding contour, an omission response appeared in the evoked potential record. We conclude that prosodic entrainment is a functional mechanism of temporal prediction in language comprehension. In general, acoustic rhythms appear to endow language for employing the brain's electrophysiological mechanisms of temporal prediction.

Impaired Cortical Tracking of Speech in Children with Developmental Language Disorder.

In developmental language disorder (DLD), learning to comprehend and express oneself with spoken language is impaired, but the reason for this remains unknown. Using millisecond-scale magnetoencephalography recordings combined with machine learning models, we investigated whether the possible neural basis of this disruption lies in poor cortical tracking of speech. The stimuli were common spoken Finnish words (e.g., dog, car, hammer) and sounds with corresponding meanings (e.g., dog bark, car engine, hammering). In both children with DLD (10 boys and 7 girls) and typically developing (TD) control children (14 boys and 3 girls), aged 10-15 years, the cortical activation to spoken words was best modeled as time-locked to the unfolding speech input at ∼100 ms latency between sound and cortical activation. Amplitude envelope (amplitude changes) and spectrogram (detailed time-varying spectral content) of the spoken words, but not other sounds, were very successfully decoded based on time-locked brain responses in bilateral temporal areas; based on the cortical responses, the models could tell at ∼75-85% accuracy which of the two sounds had been presented to the participant. However, the cortical representation of the amplitude envelope information was poorer in children with DLD compared with TD children at longer latencies (at ∼200-300 ms lag). We interpret this effect as reflecting poorer retention of acoustic-phonetic information in short-term memory. This impaired tracking could potentially affect the processing and learning of words as well as continuous speech. The present results offer an explanation for the problems in language comprehension and acquisition in DLD.

Isolating Neural Signatures of Conscious Speech Perception with a No-Report Sine-Wave Speech Paradigm.

Identifying neural correlates of conscious perception is a fundamental endeavor of cognitive neuroscience. Most studies so far have focused on visual awareness along with trial-by-trial reports of task-relevant stimuli, which can confound neural measures of perceptual awareness with postperceptual processing. Here, we used a three-phase sine-wave speech paradigm that dissociated between conscious speech perception and task relevance while recording EEG in humans of both sexes. Compared with tokens perceived as noise, physically identical sine-wave speech tokens that were perceived as speech elicited a left-lateralized, near-vertex negativity, which we interpret as a phonological version of a perceptual awareness negativity. This response appeared between 200 and 300 ms after token onset and was not present for frequency-flipped control tokens that were never perceived as speech. In contrast, the P3b elicited by task-irrelevant tokens did not significantly differ when the tokens were perceived as speech versus noise and was only enhanced for tokens that were both perceived as speech and relevant to the task. Our results extend the findings from previous studies on visual awareness and speech perception and suggest that correlates of conscious perception, across types of conscious content, are most likely to be found in midlatency negative-going brain responses in content-specific sensory areas.

Attention-Driven Modulation of Auditory Cortex Activity during Selective Listening in a Multispeaker Setting.

Real-world listening settings often consist of multiple concurrent sound streams. To limit perceptual interference during selective listening, the auditory system segregates and filters the relevant sensory input. Previous work provided evidence that the auditory cortex is critically involved in this process and selectively gates attended input toward subsequent processing stages. We studied at which level of auditory cortex processing this filtering of attended information occurs using functional magnetic resonance imaging (fMRI) and a naturalistic selective listening task. Forty-five human listeners (of either sex) attended to one of two continuous speech streams, presented either concurrently or in isolation. Functional data were analyzed using an inter-subject analysis to assess stimulus-specific components of ongoing auditory cortex activity. Our results suggest that stimulus-related activity in the primary auditory cortex and the adjacent planum temporale are hardly affected by attention, whereas brain responses at higher stages of the auditory cortex processing hierarchy become progressively more selective for the attended input. Consistent with these findings, a complementary analysis of stimulus-driven functional connectivity further demonstrated that information on the to-be-ignored speech stream is shared between the primary auditory cortex and the planum temporale but largely fails to reach higher processing stages. Our findings suggest that the neural processing of ignored speech cannot be effectively suppressed at the level of early cortical processing of acoustic features but is gradually attenuated once the competing speech streams are fully segregated.