Representation In Auditory Cortex Research Articles

Neuronal activity in sensory cortex predicts the specificity of learning in mice

Learning to avoid dangerous signals while preserving normal responses to safe stimuli is essential for everyday behavior and survival. Following identical experiences, subjects exhibit fear specificity ranging from high (specializing fear to only the dangerous stimulus) to low (generalizing fear to safe stimuli), yet the neuronal basis of fear specificity remains unknown. Here, we identified the neuronal code that underlies inter-subject variability in fear specificity using longitudinal imaging of neuronal activity before and after differential fear conditioning in the auditory cortex of mice. Neuronal activity prior to, but not after learning predicted the level of specificity following fear conditioning across subjects. Stimulus representation in auditory cortex was reorganized following conditioning. However, the reorganized neuronal activity did not relate to the specificity of learning. These results present a novel neuronal code that determines individual patterns in learning.

Multisensory-Guided Associative Learning Enhances Multisensory Representation in Primary Auditory Cortex.

Sensory cortices, classically considered to represent modality-specific sensory information, are also found to engage in multisensory processing. However, how sensory processing in sensory cortices is cross-modally modulated remains an open question. Specifically, we understand little of cross-modal representation in sensory cortices in perceptual tasks and how perceptual learning modifies this process. Here, we recorded neural responses in primary auditory cortex (A1) both while freely moving rats discriminated stimuli in Go/No-Go tasks and when anesthetized. Our data show that cross-modal representation in auditory cortices varies with task contexts. In the task of an audiovisual cue being the target associating with water reward, a significantly higher proportion of auditory neurons showed a visually evoked response. The vast majority of auditory neurons, if processing auditory-visual interactions, exhibit significant multisensory enhancement. However, when the rats performed tasks with unisensory cues being the target, cross-modal inhibition, rather than enhancement, predominated. In addition, multisensory associational learning appeared to leave a trace of plastic change in A1, as a larger proportion of A1 neurons showed multisensory enhancement in anesthesia. These findings indicate that multisensory processing in principle sensory cortices is not static, and having cross-modal interaction in the task requirement can substantially enhance multisensory processing in sensory cortices.

Reading-induced shifts of perceptual speech representations in auditory cortex

Learning to read requires the formation of efficient neural associations between written and spoken language. Whether these associations influence the auditory cortical representation of speech remains unknown. Here we address this question by combining multivariate functional MRI analysis and a newly-developed ‘text-based recalibration’ paradigm. In this paradigm, the pairing of visual text and ambiguous speech sounds shifts (i.e. recalibrates) the perceptual interpretation of the ambiguous sounds in subsequent auditory-only trials. We show that it is possible to retrieve the text-induced perceptual interpretation from fMRI activity patterns in the posterior superior temporal cortex. Furthermore, this auditory cortical region showed significant functional connectivity with the inferior parietal lobe (IPL) during the pairing of text with ambiguous speech. Our findings indicate that reading-related audiovisual mappings can adjust the auditory cortical representation of speech in typically reading adults. Additionally, they suggest the involvement of the IPL in audiovisual and/or higher-order perceptual processes leading to this adjustment. When applied in typical and dyslexic readers of different ages, our text-based recalibration paradigm may reveal relevant aspects of perceptual learning and plasticity during successful and failing reading development.

Compensating Level-Dependent Frequency Representation in Auditory Cortex by Synaptic Integration of Corticocortical Input.

Robust perception of auditory objects over a large range of sound intensities is a fundamental feature of the auditory system. However, firing characteristics of single neurons across the entire auditory system, like the frequency tuning, can change significantly with stimulus intensity. Physiological correlates of level-constancy of auditory representations hence should be manifested on the level of larger neuronal assemblies or population patterns. In this study we have investigated how information of frequency and sound level is integrated on the circuit-level in the primary auditory cortex (AI) of the Mongolian gerbil. We used a combination of pharmacological silencing of corticocortically relayed activity and laminar current source density (CSD) analysis. Our data demonstrate that with increasing stimulus intensities progressively lower frequencies lead to the maximal impulse response within cortical input layers at a given cortical site inherited from thalamocortical synaptic inputs. We further identified a temporally precise intercolumnar synaptic convergence of early thalamocortical and horizontal corticocortical inputs. Later tone-evoked activity in upper layers showed a preservation of broad tonotopic tuning across sound levels without shifts towards lower frequencies. Synaptic integration within corticocortical circuits may hence contribute to a level-robust representation of auditory information on a neuronal population level in the auditory cortex.

Comodulation Enhances Signal Detection via Priming of Auditory Cortical Circuits.

Acoustic environments are composed of complex overlapping sounds that the auditory system is required to segregate into discrete perceptual objects. The functions of distinct auditory processing stations in this challenging task are poorly understood. Here we show a direct role for mouse auditory cortex in detection and segregation of acoustic information. We measured the sensitivity of auditory cortical neurons to brief tones embedded in masking noise. By altering spectrotemporal characteristics of the masker, we reveal that sensitivity to pure tone stimuli is strongly enhanced in coherently modulated broadband noise, corresponding to the psychoacoustic phenomenon comodulation masking release. Improvements in detection were largest following priming periods of noise alone, indicating that cortical segregation is enhanced over time. Transient opsin-mediated silencing of auditory cortex during the priming period almost completely abolished these improvements, suggesting that cortical processing may play a direct and significant role in detection of quiet sounds in noisy environments.SIGNIFICANCE STATEMENT Auditory systems are adept at detecting and segregating competing sound sources, but there is little direct evidence of how this process occurs in the mammalian auditory pathway. We demonstrate that coherent broadband noise enhances signal representation in auditory cortex, and that prolonged exposure to noise is necessary to produce this enhancement. Using optogenetic perturbation to selectively silence auditory cortex during early noise processing, we show that cortical processing plays a crucial role in the segregation of competing sounds.

A Brain System for Auditory Working Memory

The brain basis for auditory working memory, the process of actively maintaining sounds in memory over short periods of time, is controversial. Using functional magnetic resonance imaging in human participants, we demonstrate that the maintenance of single tones in memory is associated with activation in auditory cortex. In addition, sustained activation was observed in hippocampus and inferior frontal gyrus. Multivoxel pattern analysis showed that patterns of activity in auditory cortex and left inferior frontal gyrus distinguished the tone that was maintained in memory. Functional connectivity during maintenance was demonstrated between auditory cortex and both the hippocampus and inferior frontal cortex. The data support a system for auditory working memory based on the maintenance of sound-specific representations in auditory cortex by projections from higher-order areas, including the hippocampus and frontal cortex. In this work, we demonstrate a system for maintaining sound in working memory based on activity in auditory cortex, hippocampus, and frontal cortex, and functional connectivity among them. Specifically, our work makes three advances from the previous work. First, we robustly demonstrate hippocampal involvement in all phases of auditory working memory (encoding, maintenance, and retrieval): the role of hippocampus in working memory is controversial. Second, using a pattern classification technique, we show that activity in the auditory cortex and inferior frontal gyrus is specific to the maintained tones in working memory. Third, we show long-range connectivity of auditory cortex to hippocampus and frontal cortex, which may be responsible for keeping such representations active during working memory maintenance.

Flexible Sensory Representations in Auditory Cortex Driven by Behavioral Relevance

Animals require the ability to ignore sensory stimuli that have no consequence yet respond to the same stimuli when they become useful. However, the brain circuits that govern this flexibility in sensory processing are not well understood. Here we show in mouse primary auditory cortex (A1) that daily passive sound exposure causes a long-lasting reduction in representations of the experienced sound by layer 2/3 pyramidal cells. This habituation arises locally in A1 and involves an enhancement in inhibition and selective upregulation in the activity of somatostatin-expressing inhibitory neurons (SOM cells). Furthermore, when mice engage in sound-guided behavior, pyramidal cell excitatory responses to habituated sounds are enhanced, whereas SOM cell responses are diminished. Together, our results demonstrate the bidirectional modulation of A1 sensory representations and suggest that SOM cells gate cortical information flow based on the behavioral relevance of the stimulus.

Bilinguals at the “cocktail party”: Dissociable neural activity in auditory–linguistic brain regions reveals neurobiological basis for nonnative listeners’ speech-in-noise recognition deficits

We examined a consistent deficit observed in bilinguals: poorer speech-in-noise (SIN) comprehension for their nonnative language. We recorded neuroelectric mismatch potentials in mono- and bi-lingual listeners in response to contrastive speech sounds in noise. Behaviorally, late bilinguals required ∼10dB more favorable signal-to-noise ratios to match monolinguals’ SIN abilities. Source analysis of cortical activity demonstrated monotonic increase in response latency with noise in superior temporal gyrus (STG) for both groups, suggesting parallel degradation of speech representations in auditory cortex. Contrastively, we found differential speech encoding between groups within inferior frontal gyrus (IFG)—adjacent to Broca’s area—where noise delays observed in nonnative listeners were offset in monolinguals. Notably, brain-behavior correspondences double dissociated between language groups: STG activation predicted bilinguals’ SIN, whereas IFG activation predicted monolinguals’ performance. We infer higher-order brain areas act compensatorily to enhance impoverished sensory representations but only when degraded speech recruits linguistic brain mechanisms downstream from initial auditory-sensory inputs.

How dopamine shapes representations in auditory cortex

The neural representation of sound in the auditory cortex is not invariably predetermined by its acoustical properties, but it is constantly reshaped while the listener acquires new experiences. Such plastic changes are a prerequisite for lifelong learning and allow some degree of rehabilitation after brain injuries. Several neurotransmitter systems modulate these plastic changes. In this paper, we focus on how the neurotransmitter dopamine modulates learning-related plasticity in auditory cortex, and how animal and human research can complement each other in providing an experimental approach that has relevance for studying mechanisms of recovery of function

Brief pitch-priming facilitates infants’ discrimination of pitch-evoking noise: Evidence from event-related potentials

Pitch is derived by the auditory system through complex spectrotemporal processing. Pitch extraction is thought to depend on both spectral cues arising from lower harmonics that are resolved by cochlear filters in the inner ear, and on temporal cues arising from the pattern of action potentials contained in the cochlear output. Adults are capable of extracting pitch in the absence of robust spectral cues, taking advantage of the temporal cues that remain. However, recent behavioral evidence suggests that infants have difficulty discriminating between stimuli with different pitches when resolvable spectral cues are absent. In the current experiments, we used the mismatch negativity (MMN) component of the event related potential derived from electroencephalographic (EEG) recordings to examine a cortical representation of pitch discrimination for iterated rippled noise (IRN) stimuli in 4- and 8-month-old infants. IRN stimuli are pitch-evoking sounds generated by repeatedly adding a segment of white noise to itself at a constant delay. We created IRN stimuli (delays of 5 and 6ms creating pitch percepts of 200 and 167Hz) and high-pass filtered them to remove all resolvable spectral pitch cues. In experiment 1, we did not find EEG evidence that infants could detect the change in the pitch of these IRN stimuli. However, in Experiment 2, after a brief period of pitch-priming during which we added a sine wave component to the IRN stimulus at its perceived pitch, infants did show significant MMN in response to pitch changes in the IRN stimuli with sine waves removed. This suggests that (1) infants can use temporal cues to process pitch, although such processing is not mature and (2) that a short amount of pitch-priming experience can alter pitch representations in auditory cortex during infancy.

Seeing Is Believing: Neural Representations of Visual Stimuli in Human Auditory Cortex Correlate with Illusory Auditory Perceptions

In interpersonal communication, the listener can often see as well as hear the speaker. Visual stimuli can subtly change a listener’s auditory perception, as in the McGurk illusion, in which perception of a phoneme’s auditory identity is changed by a concurrent video of a mouth articulating a different phoneme. Studies have yet to link visual influences on the neural representation of language with subjective language perception. Here we show that vision influences the electrophysiological representation of phonemes in human auditory cortex prior to the presentation of the auditory stimulus. We used the McGurk effect to dissociate the subjective perception of phonemes from the auditory stimuli. With this paradigm we demonstrate that neural representations in auditory cortex are more closely correlated with the visual stimuli of mouth articulation, which drive the illusory subjective auditory perception, than the actual auditory stimuli. Additionally, information about visual and auditory stimuli transfer in the caudal–rostral direction along the superior temporal gyrus during phoneme perception as would be expected of visual information flowing from the occipital cortex into the ventral auditory processing stream. These results show that visual stimuli influence the neural representation in auditory cortex early in sensory processing and may override the subjective auditory perceptions normally generated by auditory stimuli. These findings depict a marked influence of vision on the neural processing of audition in tertiary auditory cortex and suggest a mechanistic underpinning for the McGurk effect.

A Comprehensive Three-dimensional Cortical Map of Vowel Space

Mammalian cortex is known to contain various kinds of spatial encoding schemes for sensory information including retinotopic, somatosensory, and tonotopic maps. Tonotopic maps are especially interesting for human speech sound processing because they encode linguistically salient acoustic properties. In this study, we mapped the entire vowel space of a language (Turkish) onto cortical locations by using the magnetic N1 (M100), an auditory-evoked component that peaks approximately 100 msec after auditory stimulus onset. We found that dipole locations could be structured into two distinct maps, one for vowels produced with the tongue positioned toward the front of the mouth (front vowels) and one for vowels produced in the back of the mouth (back vowels). Furthermore, we found spatial gradients in lateral-medial, anterior-posterior, and inferior-superior dimensions that encoded the phonetic, categorical distinctions between all the vowels of Turkish. Statistical model comparisons of the dipole locations suggest that the spatial encoding scheme is not entirely based on acoustic bottom-up information but crucially involves featural-phonetic top-down modulation. Thus, multiple areas of excitation along the unidimensional basilar membrane are mapped into higher dimensional representations in auditory cortex.

Tracking Vocal Pitch through Noise: Neural Correlates in Nonprimary Auditory Cortex

In natural environments, a sound can be heard as stable despite the presence of other occasionally louder sounds. For example, when a portion in a voice is replaced by masking noise, the interrupted voice may still appear illusorily continuous. Previous research found that continuity illusions of simple interrupted sounds, such as tones, are accompanied by weaker activity in the primary auditory cortex (PAC) during the interruption than veridical discontinuity percepts of these sounds. Here, we studied whether continuity illusions of more natural and more complex sounds also emerge from this mechanism. We used psychophysics and functional magnetic resonance imaging in humans to measure simultaneously continuity ratings and blood oxygenation level-dependent activity to vowels that were partially replaced by masking noise. Consistent with previous results on tone continuity illusions, we found listeners' reports of more salient vowel continuity illusions associated with weaker activity in auditory cortex (compared with reports of veridical discontinuity percepts of physically identical stimuli). In contrast to the reduced activity to tone continuity illusions in PAC, this reduction was localized in the right anterolateral Heschl's gyrus, a region that corresponds more to the non-PAC. Our findings suggest that the ability to hear differently complex sounds as stable during other louder sounds may be attributable to a common suppressive mechanism that operates at different levels of sound representation in auditory cortex.

Attentional Gain Control of Ongoing Cortical Speech Representations in a “Cocktail Party”

Normal listeners possess the remarkable perceptual ability to select a single speech stream among many competing talkers. However, few studies of selective attention have addressed the unique nature of speech as a temporally extended and complex auditory object. We hypothesized that sustained selective attention to speech in a multitalker environment would act as gain control on the early auditory cortical representations of speech. Using high-density electroencephalography and a template-matching analysis method, we found selective gain to the continuous speech content of an attended talker, greatest at a frequency of 4-8 Hz, in auditory cortex. In addition, the difference in alpha power (8-12 Hz) at parietal sites across hemispheres indicated the direction of auditory attention to speech, as has been previously found in visual tasks. The strength of this hemispheric alpha lateralization, in turn, predicted an individual's attentional gain of the cortical speech signal. These results support a model of spatial speech stream segregation, mediated by a supramodal attention mechanism, enabling selection of the attended representation in auditory cortex.

Visual influences on information representations in auditory cortex

Visual influences on information representations in auditory cortex

Visual Enhancement of the Information Representation in Auditory Cortex

Combining information across different sensory modalities can greatly facilitate our ability to detect, discriminate, or recognize sensory stimuli. Although this process of sensory integration has usually been attributed to classical association cortices, recent work has demonstrated that neuronal activity in early sensory cortices can also be influenced by cross-modal inputs. Here we demonstrate that such "early" multisensory influences enhance the information carried by neurons about multisensory stimuli. By recording in auditory cortex of alert monkeys watching naturalistic audiovisual stimuli, we quantified the effect of visual influences on the trial-to-trial response variability and on the amount of information carried by neural responses. We found that firing rates and precisely timed spike patterns of individual units became more reliable across trials and time when multisensory stimuli were presented, leading to greater encoded stimulus information. Importantly, this multisensory information enhancement was much reduced when the visual stimulus did not match the sound. These results demonstrate that multisensory influences enhance information processing already at early stages in cortex, suggesting that sensory integration is a distributed process, commencing in lower sensory areas and continuing in higher association cortices.

Auditory‐Somatosensory Integration and Cortical Plasticity in Musical Training

Learning to play a musical instrument requires complex multimodal skills involving simultaneous perception of several sensory modalities: auditory, visual, and somatosensory as well as the motor system. Musical training thus provides an adequate neuroscientific model to study multimodal integration and plasticity in musical training. The aim of this study was to investigate the impact of short-term uni- and multimodal musical training on auditory-somatosensory integration and plasticity. Two groups of nonmusicians were musically trained. The first group (sensorimotor-auditory group, SA) learned to play a musical sequence on the piano, whereas the second one (auditory group, A) actively listened to and made judgments about the correctness of the music. The training-induced cortical plasticity effect was assessed by recording musically elicited mismatch negativity (MMN) from magnetoencephalographic (MEG) measurements before and after training. The SA group showed significant enlargement of MMN after training compared to the A group, reflecting greater enhancement of musical representations in auditory cortex after sensorimotor-auditory training compared to mere auditory training. This study demonstrates that the sensorimotor and auditory systems integrate and that this multimodal training causes cortical reorganizational changes in the auditory cortex over and above the changes introduced by auditory training alone.

Sensitivity to interaural level differences in high‐rate high‐frequency click trains: A functional magnetic resonance imaging assessment.

While the auditory cortex (AC) is known to be necessary for accurate sound localization, the nature of spatial representation in AC remains poorly understood. Past animal studies have quantified sensitivity to auditory spatial cues [e.g., interaural level difference (ILD)] across subregions of AC. In this study, functional magnetic resonance imaging (fMRI) was used to assess ILD sensitivity across the surface of human AC. Normal‐hearing listeners were presented with narrowband Gabor click trains (4000 Hz center frequency, 3 ms interclick interval) that varied parametrically in ILD over a range of +/− 30 dB. Simultaneously, whole‐head fMRI images were acquired using a sparse imaging paradigm at 3 Tesla (32‐slice EPI, 3.0×3.0×4.5 mm resolution, TR=12 s). During imaging, listeners detected rare target changes in ICI. Hemodynamic responses of compact AC subregions in individual subjects were assessed quantitatively using statistical pattern recognition with two goals: (1) to identify contiguous AC regions that share common patterns of sensitivity to ILD, and (2) to quantify, in information‐theoretic terms, the ability of those responses to differentiate stimuli differing in ILD.

Cortical Plasticity Induced by Short-Term Unimodal and Multimodal Musical Training

Learning to play a musical instrument requires complex multimodal skills involving simultaneous perception of several sensory modalities: auditory, visual, somatosensory, as well as the motor system. Therefore, musical training provides a good and adequate neuroscientific model to study multimodal brain plasticity effects in humans. Here, we investigated the impact of short-term unimodal and multimodal musical training on brain plasticity. Two groups of nonmusicians were musically trained over the course of 2 weeks. One group [sensorimotor-auditory (SA)] learned to play a musical sequence on the piano, whereas the other group [auditory (A)] listened to and made judgments about the music that had been played by participants of the sensorimotor-auditory group. Training-induced cortical plasticity was assessed by recording the musically elicited mismatch negativity (MMNm) from magnetoencephalographic measurements before and after training. SA and A groups showed significantly different cortical responses after training. Specifically, the SA group showed significant enlargement of MMNm after training compared with the A group, reflecting greater enhancement of musical representations in auditory cortex after sensorimotor-auditory training compared with after mere auditory training. Thus, we have experimentally demonstrated that not only are sensorimotor and auditory systems connected, but also that sensorimotor-auditory training causes plastic reorganizational changes in the auditory cortex over and above changes introduced by auditory training alone.

Cerebral Responses to Change in Spatial Location of Unattended Sounds

The neural basis of spatial processing in the auditory cortex has been controversial. Human fMRI studies suggest that a part of the planum temporale (PT) is involved in auditory spatial processing, but it was recently argued that this region is active only when the task requires voluntary spatial localization. If this is the case, then this region cannot harbor an ongoing spatial representation of the acoustic environment. In contrast, we show in three fMRI experiments that a region in the human medial PT is sensitive to background auditory spatial changes, even when subjects are not engaged in a spatial localization task, and in fact attend the visual modality. During such times, this area responded to rare location shifts, and even more so when spatial variation increased, consistent with spatially selective adaptation. Thus, acoustic space is represented in the human PT even when sound processing is not required by the ongoing task.