Non-primary Auditory Cortex Research Articles

FMRI speech tracking in primary and non-primary auditory cortex while listening to noisy scenes

Invasive and non-invasive electrophysiological measurements during “cocktail-party”-like listening indicate that neural activity in the human auditory cortex (AC) “tracks” the envelope of relevant speech. However, due to limited coverage and/or spatial resolution, the distinct contribution of primary and non-primary areas remains unclear. Here, using 7-Tesla fMRI, we measured brain responses of participants attending to one speaker, in the presence and absence of another speaker. Through voxel-wise modeling, we observed envelope tracking in bilateral Heschl’s gyrus (HG), right middle superior temporal sulcus (mSTS) and left temporo-parietal junction (TPJ), despite the signal’s sluggish nature and slow temporal sampling. Neurovascular activity correlated positively (HG) or negatively (mSTS, TPJ) with the envelope. Further analyses comparing the similarity between spatial response patterns in the single speaker and concurrent speakers conditions and envelope decoding indicated that tracking in HG reflected both relevant and (to a lesser extent) non-relevant speech, while mSTS represented the relevant speech signal. Additionally, in mSTS, the similarity strength correlated with the comprehension of relevant speech. These results indicate that the fMRI signal tracks cortical responses and attention effects related to continuous speech and support the notion that primary and non-primary AC process ongoing speech in a push-pull of acoustic and linguistic information.

Task-specific invariant representation in auditory cortex.

Categorical sensory representations are critical for many behaviors, including speech perception. In the auditory system, categorical information is thought to arise hierarchically, becoming increasingly prominent in higher-order cortical regions. The neural mechanisms that support this robust and flexible computation remain poorly understood. Here, we studied sound representations in the ferret primary and non-primary auditory cortex while animals engaged in a challenging sound discrimination task. Population-level decoding of simultaneously recorded single neurons revealed that task engagement caused categorical sound representations to emerge in non-primary auditory cortex. In primary auditory cortex, task engagement caused a general enhancement of sound decoding that was not specific to task-relevant categories. These findings are consistent with mixed selectivity models of neural disentanglement, in which early sensory regions build an overcomplete representation of the world and allow neurons in downstream brain regions to flexibly and selectively read out behaviorally relevant, categorical information.

Functional Connectivity of the Auditory Cortex in Women With Trauma-Related Disorders Who Hear Voices

BackgroundVoice hearing (VH) is a transdiagnostic experience that is common in trauma-related disorders. However, the neural substrates that underlie trauma-related VH remain largely unexplored. While auditory perceptual dysfunction is among the abnormalities implicated in VH in schizophrenia, whether VH in trauma-related disorders also involves auditory perceptual alterations is unknown. MethodsWe investigated auditory cortex (AC)–related functional connectivity (FC) in 65 women with trauma-related disorders stemming from childhood abuse with varying severities of VH. Using a novel, computationally driven and individual-specific method of functionally parcellating the brain, we calculated the FC of 2 distinct AC subregions—Heschl’s gyrus (corresponding to the primary AC) and lateral superior temporal gyrus (in the nonprimary AC)—with both the cerebrum and cerebellum. Then, we measured the association between VH severity and FC using leave-one-out cross-validation in the cerebrum and voxelwise multiple regression analyses in the cerebellum. ResultsWe found that VH severity was positively correlated with left lateral superior temporal gyrus–frontoparietal network FC, while it was negatively correlated with FC between the left lateral superior temporal gyrus and both cerebral and cerebellar representations of the default mode network. VH severity was not predicted by FC of the left Heschl’s gyrus or right AC subregions. ConclusionsOur findings point to altered interactions between auditory perceptual processing and higher-level processes related to self-reference and executive functioning. This is the first study to show alterations in auditory cortical connectivity in trauma-related VH. While VH in trauma-related disorders appears to be mediated by brain networks that are also implicated in VH in schizophrenia, the results suggest a unique mechanism that could distinguish VH in trauma-related disorders.

Mouse auditory cortex sub-fields receive neuronal projections from MGB subdivisions independently

Mouse auditory cortex is composed of six sub-fields: primary auditory field (AI), secondary auditory field (AII), anterior auditory field (AAF), insular auditory field (IAF), ultrasonic field (UF) and dorsoposterior field (DP). Previous studies have examined thalamo-cortical connections in the mice auditory system and learned that AI, AAF, and IAF receive inputs from the ventral division of the medial geniculate body (MGB). However, the functional and thalamo-cortical connections between nonprimary auditory cortex (AII, UF, and DP) is unclear. In this study, we examined the locations of neurons projecting to these three cortical sub-fields in the MGB, and addressed the question whether these cortical sub-fields receive inputs from different subsets of MGB neurons or common. To examine the distributions of projecting neurons in the MGB, retrograde tracers were injected into the AII, UF, DP, after identifying these areas by the method of Optical Imaging. Our results indicated that neuron cells which in ventral part of dorsal MGB (MGd) and that of ventral MGB (MGv) projecting to UF and AII with less overlap. And DP only received neuron projecting from MGd. Interestingly, these three cortical areas received input from distinct part of MGd and MGv in an independent manner. Based on our foundings these three auditory cortical sub-fields in mice may independently process auditory information.

Population coding of time-varying sounds in the nonlemniscal inferior colliculus.

The inferior colliculus (IC) of the midbrain is important for complex sound processing, such as discriminating conspecific vocalizations and human speech. The IC's nonlemniscal, dorsal "shell" region is likely important for this process, as neurons in these layers project to higher-order thalamic nuclei that subsequently funnel acoustic signals to the amygdala and nonprimary auditory cortices, forebrain circuits important for vocalization coding in a variety of mammals, including humans. However, the extent to which shell IC neurons transmit acoustic features necessary to discern vocalizations is less clear, owing to the technical difficulty of recording from neurons in the IC's superficial layers via traditional approaches. Here, we use two-photon Ca2+ imaging in mice of either sex to test how shell IC neuron populations encode the rate and depth of amplitude modulation, important sound cues for speech perception. Most shell IC neurons were broadly tuned, with a low neurometric discrimination of amplitude modulation rate; only a subset was highly selective to specific modulation rates. Nevertheless, neural network classifier trained on fluorescence data from shell IC neuron populations accurately classified amplitude modulation rate, and decoding accuracy was only marginally reduced when highly tuned neurons were omitted from training data. Rather, classifier accuracy increased monotonically with the modulation depth of the training data, such that classifiers trained on full-depth modulated sounds had median decoding errors of ∼0.2 octaves. Thus, shell IC neurons may transmit time-varying signals via a population code, with perhaps limited reliance on the discriminative capacity of any individual neuron.NEW & NOTEWORTHY The IC's shell layers originate a "nonlemniscal" pathway important for perceiving vocalization sounds. However, prior studies suggest that individual shell IC neurons are broadly tuned and have high response thresholds, implying a limited reliability of efferent signals. Using Ca2+ imaging, we show that amplitude modulation is accurately represented in the population activity of shell IC neurons. Thus, downstream targets can read out sounds' temporal envelopes from distributed rate codes transmitted by populations of broadly tuned neurons.

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 convolutional neural network provides a generalizable model of natural sound coding by neural populations in auditory cortex.

Convolutional neural networks (CNNs) can provide powerful and flexible models of neural sensory processing. However, the utility of CNNs in studying the auditory system has been limited by their requirement for large datasets and the complex response properties of single auditory neurons. To address these limitations, we developed a population encoding model: a CNN that simultaneously predicts activity of several hundred neurons recorded during presentation of a large set of natural sounds. This approach defines a shared spectro-temporal space and pools statistical power across neurons. Population models of varying architecture performed consistently and substantially better than traditional linear-nonlinear models on data from primary and non-primary auditory cortex. Moreover, population models were highly generalizable. The output layer of a model pre-trained on one population of neurons could be fit to data from novel single units, achieving performance equivalent to that of neurons in the original fit data. This ability to generalize suggests that population encoding models capture a complete representational space across neurons in an auditory cortical field.

Deep neural networks effectively model neural adaptation to changing background noise and suggest nonlinear noise filtering methods in auditory cortex

The human auditory system displays a robust capacity to adapt to sudden changes in background noise, allowing for continuous speech comprehension despite changes in background environments. However, despite comprehensive studies characterizing this ability, the computations that underly this process are not well understood. The first step towards understanding a complex system is to propose a suitable model, but the classical and easily interpreted model for the auditory system, the spectro-temporal receptive field (STRF), cannot match the nonlinear neural dynamics involved in noise adaptation. Here, we utilize a deep neural network (DNN) to model neural adaptation to noise, illustrating its effectiveness at reproducing the complex dynamics at the levels of both individual electrodes and the cortical population. By closely inspecting the model's STRF-like computations over time, we find that the model alters both the gain and shape of its receptive field when adapting to a sudden noise change. We show that the DNN model's gain changes allow it to perform adaptive gain control, while the spectro-temporal change creates noise filtering by altering the inhibitory region of the model's receptive field. Further, we find that models of electrodes in nonprimary auditory cortex also exhibit noise filtering changes in their excitatory regions, suggesting differences in noise filtering mechanisms along the cortical hierarchy. These findings demonstrate the capability of deep neural networks to model complex neural adaptation and offer new hypotheses about the computations the auditory cortex performs to enable noise-robust speech perception in real-world, dynamic environments.

Intact speech perception after resection of dominant hemisphere primary auditory cortex for the treatment of medically refractory epilepsy: illustrative case.

In classic speech network models, the primary auditory cortex is the source of auditory input to Wernicke's area in the posterior superior temporal gyrus (pSTG). Because resection of the primary auditory cortex in the dominant hemisphere removes inputs to the pSTG, there is a risk of speech impairment. However, recent research has shown the existence of other, nonprimary auditory cortex inputs to the pSTG, potentially reducing the risk of primary auditory cortex resection in the dominant hemisphere. Here, the authors present a clinical case of a woman with severe medically refractory epilepsy with a lesional epileptic focus in the left (dominant) Heschl's gyrus. Analysis of neural responses to speech stimuli was consistent with primary auditory cortex localization to Heschl's gyrus. Although the primary auditory cortex was within the proposed resection margins, she underwent lesionectomy with total resection of Heschl's gyrus. Postoperatively, she had no speech deficits and her seizures were fully controlled. While resection of the dominant hemisphere Heschl's gyrus/primary auditory cortex warrants caution, this case illustrates the ability to resect the primary auditory cortex without speech impairment and supports recent models of multiple parallel inputs to the pSTG.

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.

Cerebral Representation of Sound Localization Using Functional Near-Infrared Spectroscopy.

Sound localization is an essential part of auditory processing. However, the cortical representation of identifying the direction of sound sources presented in the sound field using functional near-infrared spectroscopy (fNIRS) is currently unknown. Therefore, in this study, we used fNIRS to investigate the cerebral representation of different sound sources. Twenty-five normal-hearing subjects (aged 26 ± 2.7, male 11, female 14) were included and actively took part in a block design task. The test setup for sound localization was composed of a seven-speaker array spanning a horizontal arc of 180° in front of the participants. Pink noise bursts with two intensity levels (48 dB/58 dB) were randomly applied via five loudspeakers (–90°/–30°/–0°/+30°/+90°). Sound localization task performances were collected, and simultaneous signals from auditory processing cortical fields were recorded for analysis by using a support vector machine (SVM). The results showed a classification accuracy of 73.60, 75.60, and 77.40% on average at –90°/0°, 0°/+90°, and –90°/+90° with high intensity, and 70.60, 73.6, and 78.6% with low intensity. The increase of oxyhemoglobin was observed in the bilateral non-primary auditory cortex (AC) and dorsolateral prefrontal cortex (dlPFC). In conclusion, the oxyhemoglobin (oxy-Hb) response showed different neural activity patterns between the lateral and front sources in the AC and dlPFC. Our results may serve as a basic contribution for further research on the use of fNIRS in spatial auditory studies.

Distinct higher-order representations of natural sounds in human and ferret auditory cortex.

Little is known about how neural representations of natural sounds differ across species. For example, speech and music play a unique role in human hearing, yet it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional ultrasound imaging, we measured responses in ferrets to a set of natural and spectrotemporally matched synthetic sounds previously tested in humans. Ferrets showed similar lower-level frequency and modulation tuning to that observed in humans. But while humans showed substantially larger responses to natural vs. synthetic speech and music in non-primary regions, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary auditory cortex, even when tested with ferret vocalizations. This finding reveals that auditory representations in humans and ferrets diverge sharply at late stages of cortical processing, potentially driven by higher-order processing demands in speech and music.

Speech Computations of the Human Superior Temporal Gyrus.

Human speech perception results from neural computations that transform external acoustic speech signals into internal representations of words. The superior temporal gyrus (STG) contains the nonprimary auditory cortex and is a critical locus for phonological processing. Here, we describe how speech sound representation in the STG relies on fundamentally nonlinear and dynamical processes, such as categorization, normalization, contextual restoration, and the extraction of temporal structure. A spatial mosaic of local cortical sites on the STG exhibits complex auditory encoding for distinct acoustic-phonetic and prosodic features. We propose that as a population ensemble, these distributed patterns of neural activity give rise to abstract, higher-order phonemic and syllabic representations that support speech perception. This review presents a multi-scale, recurrent model of phonological processing in the STG, highlighting the critical interface between auditory and language systems.

Parallel and distributed encoding of speech across human auditory cortex

Speech perception is thought to rely on a cortical feedforward serial transformation of acoustic into linguistic representations. Using intracranial recordings across the entire human auditory cortex, electrocortical stimulation, and surgical ablation, we show that cortical processing across areas is not consistent with a serial hierarchical organization. Instead, response latency and receptive field analyses demonstrate parallel and distinct information processing in the primary and nonprimary auditory cortices. This functional dissociation was also observed where stimulation of the primary auditory cortex evokes auditory hallucination but does not distort or interfere with speech perception. Opposite effects were observed during stimulation of nonprimary cortex in superior temporal gyrus. Ablation of the primary auditory cortex does not affect speech perception. These results establish a distributed functional organization of parallel information processing throughout the human auditory cortex and demonstrate an essential independent role for nonprimary auditory cortex in speech processing.

Neuronal figure-ground responses in primate primary auditory cortex.

SummaryFigure-ground segregation, the brain’s ability to group related features into stable perceptual entities, is crucial for auditory perception in noisy environments. The neuronal mechanisms for this process are poorly understood in the auditory system. Here, we report figure-ground modulation of multi-unit activity (MUA) in the primary and non-primary auditory cortex of rhesus macaques. Across both regions, MUA increases upon presentation of auditory figures, which consist of coherent chord sequences. We show increased activity even in the absence of any perceptual decision, suggesting that neural mechanisms for perceptual grouping are, to some extent, independent of behavioral demands. Furthermore, we demonstrate differences in figure encoding between more anterior and more posterior regions; perceptual saliency is represented in anterior cortical fields only. Our results suggest an encoding of auditory figures from the earliest cortical stages by a rate code.

From acoustic to linguistic analysis of temporal speech structure: Acousto-linguistic transformation during speech perception using speech quilts

Speech perception entails the mapping of the acoustic waveform to linguistic representations. For this transformation to succeed, the speech signal needs to be tracked over various temporal windows at high temporal precision in order to decode linguistic units ranging from phonemes (tens of milliseconds) to sentences (seconds). Here, we tested the hypothesis that cortical processing of speech-specific temporal structure is modulated by higher-level linguistic analysis. Using fMRI, we measured BOLD signal changes to 4 s long speech quilts with variable temporal structure (30, 120, 480, 960 ms segment lengths), as well as natural speech, created from a familiar (English) or foreign (Korean) language. We found evidence for the acoustic analysis of temporal speech properties in superior temporal sulcus (STS): the BOLD signal increased as a function of temporal speech structure in both familiar and foreign languages. However, activity in left inferior gyrus (IFG) revealed evidence for linguistic processing of temporal speech properties: the BOLD signal increased as a function of temporal speech structure only in familiar, but not in foreign speech. Network connectivity analyses suggested that left IFG modulates the processing of temporal speech structure in primary and non-primary auditory cortex, which in turn sensitizes the analysis of temporal speech structure in STS. The results thus suggest that acousto-linguistic transformation of temporal speech structure is achieved by a cortical network comprising primary and non-primary auditory cortex, STS, and left IFG.

Human cortical encoding of pitch in tonal and non-tonal languages

Languages can use a common repertoire of vocal sounds to signify distinct meanings. In tonal languages, such as Mandarin Chinese, pitch contours of syllables distinguish one word from another, whereas in non-tonal languages, such as English, pitch is used to convey intonation. The neural computations underlying language specialization in speech perception are unknown. Here, we use a cross-linguistic approach to address this. Native Mandarin- and English- speaking participants each listened to both Mandarin and English speech, while neural activity was directly recorded from the non-primary auditory cortex. Both groups show language-general coding of speaker-invariant pitch at the single electrode level. At the electrode population level, we find language-specific distribution of cortical tuning parameters in Mandarin speakers only, with enhanced sensitivity to Mandarin tone categories. Our results show that speech perception relies upon a shared cortical auditory feature processing mechanism, which may be tuned to the statistics of a given language.

The Dialog of Primary and Non-primary Auditory Cortex at the ‘Cocktail Party’

In this issue of Neuron, O'Sullivan etal. (2019) measured electro-cortical responses to "cocktail party" speech mixtures in neurosurgical patients and demonstrated that the selective enhancement of attended speech is achieved through the adaptive weighting of primary auditory cortex output by non-primary auditory cortex.

Hierarchical Encoding of Attended Auditory Objects in Multi-talker Speech Perception

Humans can easily focus on one speaker in a multi-talker acoustic environment, but how different areas of the human auditory cortex (AC) represent the acoustic components of mixed speech is unknown. We obtained invasive recordings from the primary and nonprimary AC in neurosurgical patients as they listened to multi-talker speech. We found that neural sites in the primary AC responded to individual speakers in the mixture and were relatively unchanged by attention. In contrast, neural sites in the nonprimary AC were less discerning of individual speakers but selectively represented the attended speaker. Moreover, the encoding of the attended speaker in the nonprimary AC was invariant to the degree of acoustic overlap with the unattended speaker. Finally, this emergent representation of attended speech in the nonprimary AC was linearly predictable from the primary AC responses. Our results reveal the neural computations underlying the hierarchical formation of auditory objects in human AC during multi-talker speech perception.

A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex.

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced high-frequency (70–150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however, their distribution within auditory cortex has not been established. Alpha activity (7–14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (4 female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function.SIGNIFICANCE STATEMENT To understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7–14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschl's gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.