Functional architecture of auditory cortex

Three complementary approaches demonstrate new types of organization in rodent, feline and primate auditory cortex, as well as differences in processing between auditory and visual cortex. First, connectional work reveals patterns of thalamocortical and corticocortical input unique to the auditory cortex. Second, physiological studies find multiple, interleaved auditory processing modules related to corticocortical connections and embedded in the isofrequency gradient. Third, functional analyses demonstrate independent processing streams for sound localization and identification analogous to the 'what' and 'where' streams in visual cortex, although the modular arrangements are modality-specific. Taken together, these data show that the auditory cortex has common and unique functional substrates.     

An fMRI Study of Audiovisual Speech Perception Reveals Multisensory Interactions in Auditory Cortex

Research on the neural basis of speech-reading implicates a network of auditory language regions involving inferior frontal cortex, premotor cortex and sites along superior temporal cortex. In audiovisual speech studies, neural activity is consistently reported in posterior superior temporal Sulcus (pSTS) and this site has been implicated in multimodal integration. Traditionally, multisensory interactions are considered high-level processing that engages heteromodal association cortices (such as STS). Recent work, however, challenges this notion and suggests that multisensory interactions may occur in low-level unimodal sensory cortices. While previous audiovisual speech studies demonstrate that high-level multisensory interactions occur in pSTS, what remains unclear is how early in the processing hierarchy these multisensory interactions may occur. The goal of the present fMRI experiment is to investigate how visual speech can influence activity in auditory cortex above and beyond its response to auditory speech. In an audiovisual speech experiment, subjects were presented with auditory speech with and without congruent visual input. Holding the auditory stimulus constant across the experiment, we investigated how the addition of visual speech influences activity in auditory cortex. We demonstrate that congruent visual speech increases the activity in auditory cortex.     

The signs of silence

How does auditory cortex respond to silence? In this issue of Neuron, show that activity in macaque auditory cortex is highly structured even in the absence of sensory stimuli. These data reveal a close link between spontaneous neural activity and the functional organization of auditory cortex.     

Fear conditioning induces guinea pig auditory cortex activation by foot shock alone

The present study used an optical imaging paradigm to investigate plastic changes in the auditory cortex induced by fear conditioning, in which a sound (conditioned stimulus, CS) was paired with an electric foot-shock (unconditioned stimulus, US). We report that, after conditioning, auditory information could be retrieved on the basis of an electric foot-shock alone. Before conditioning, the auditory cortex showed no response to a foot-shock presented in the absence of sound. In contrast, after conditioning, the mere presentation of a foot-shock without any sound succeeded in eliciting activity in the auditory cortex. Additionally, the magnitude of the optical response in the auditory cortex correlated with variation in the electrocardiogram (correlation coefficient: −0.68). The area activated in the auditory cortex, in response to the electric foot-shock, statistically significantly had a larger cross-correlation value for tone response to the CS sound (12 kHz) compared to the non-CS sounds in normal conditioning group. These results suggest that integration of different sensory modalities in the auditory cortex was established by fear conditioning.     

Primary auditory cortex of cats: feature detection or something else?

Neurons in sensory cortices are often assumed to be feature detectors, computing simple and then successively more complex features out of the incoming sensory stream. These features are somehow integrated into percepts. Despite many years of research, a convincing candidate for such a feature in primary auditory cortex has not been found. We argue that feature detection is actually a secondary issue in understanding the role of primary auditory cortex. Instead, the major contribution of primary auditory cortex to auditory perception is in processing previously derived features on a number of different timescales. We hypothesize that, as a result, neurons in primary auditory cortex represent sounds in terms of auditory objects rather than in terms of feature maps. According to this hypothesis, primary auditory cortex has a pivotal role in the auditory system in that it generates the representation of auditory objects to which higher auditory centers assign properties such as spatial location, source identity, and meaning.Abbreviations A1 primary auditory cortex - MGB medical geniculate body - IC inferior coliculus - STRF spectrotemporal receptive field     

Functional imaging reveals numerous fields in the monkey auditory cortex

Anatomical studies propose that the primate auditory cortex contains more fields than have actually been functionally confirmed or described. Spatially resolved functional magnetic resonance imaging (fMRI) with carefully designed acoustical stimulation could be ideally suited to extend our understanding of the processing within these fields. However, after numerous experiments in humans, many auditory fields remain poorly characterized. Imaging the macaque monkey is of particular interest as these species have a richer set of anatomical and neurophysiological data to clarify the source of the imaged activity. We functionally mapped the auditory cortex of behaving and of anesthetized macaque monkeys with high resolution fMRI. By optimizing our imaging and stimulation procedures, we obtained robust activity throughout auditory cortex using tonal and band-passed noise sounds. Then, by varying the frequency content of the sounds, spatially specific activity patterns were observed over this region. As a result, the activity patterns could be assigned to many auditory cortical fields, including those whose functional properties were previously undescribed. The results provide an extensive functional tessellation of the macaque auditory cortex and suggest that 11 fields contain neurons tuned for the frequency of sounds. This study provides functional support for a model where three fields in primary auditory cortex are surrounded by eight neighboring “belt” fields in non-primary auditory cortex. The findings can now guide neurophysiological recordings in the monkey to expand our understanding of the processing within these fields. Additionally, this work will improve fMRI investigations of the human auditory cortex.     

Cholecystokinin from the entorhinal cortex enables neural plasticity in the auditory cortex

Patients with damage to the medial temporal lobe show deficits in forming new declarative memories but can still recall older memories, suggesting that the medial temporal lobe is necessary for encoding memories in the neocortex. Here, we found that cortical projection neurons in the perirhinal and entorhinal cortices were mostly immunopositive for cholecystokinin (CCK). Local infusion of CCK in the auditory cortex of anesthetized rats induced plastic changes that enabled cortical neurons to potentiate their responses or to start responding to an auditory stimulus that was paired with a tone that robustly triggered action potentials. CCK infusion also enabled auditory neurons to start responding to a light stimulus that was paired with a noise burst. In vivo intracellular recordings in the auditory cortex showed that synaptic strength was potentiated after two pairings of presynaptic and postsynaptic activity in the presence of CCK. Infusion of a CCK_B antagonist in the auditory cortex prevented the formation of a visuo-auditory association in awake rats. Finally, activation of the entorhinal cortex potentiated neuronal responses in the auditory cortex, which was suppressed by infusion of a CCK_B antagonist. Together, these findings suggest that the medial temporal lobe influences neocortical plasticity via CCK-positive cortical projection neurons in the entorhinal cortex.     

Auditory cortex basal activity modulates cochlear responses in chinchillas

Background

The auditory efferent system has unique neuroanatomical pathways that connect the cerebral cortex with sensory receptor cells. Pyramidal neurons located in layers V and VI of the primary auditory cortex constitute descending projections to the thalamus, inferior colliculus, and even directly to the superior olivary complex and to the cochlear nucleus. Efferent pathways are connected to the cochlear receptor by the olivocochlear system, which innervates outer hair cells and auditory nerve fibers. The functional role of the cortico-olivocochlear efferent system remains debated. We hypothesized that auditory cortex basal activity modulates cochlear and auditory-nerve afferent responses through the efferent system.

Methodology/Principal Findings

Cochlear microphonics (CM), auditory-nerve compound action potentials (CAP) and auditory cortex evoked potentials (ACEP) were recorded in twenty anesthetized chinchillas, before, during and after auditory cortex deactivation by two methods: lidocaine microinjections or cortical cooling with cryoloops. Auditory cortex deactivation induced a transient reduction in ACEP amplitudes in fifteen animals (deactivation experiments) and a permanent reduction in five chinchillas (lesion experiments). We found significant changes in the amplitude of CM in both types of experiments, being the most common effect a CM decrease found in fifteen animals. Concomitantly to CM amplitude changes, we found CAP increases in seven chinchillas and CAP reductions in thirteen animals. Although ACEP amplitudes were completely recovered after ninety minutes in deactivation experiments, only partial recovery was observed in the magnitudes of cochlear responses.

Conclusions/Significance

These results show that blocking ongoing auditory cortex activity modulates CM and CAP responses, demonstrating that cortico-olivocochlear circuits regulate auditory nerve and cochlear responses through a basal efferent tone. The diversity of the obtained effects suggests that there are at least two functional pathways from the auditory cortex to the cochlea.     

The sensory consequences of speaking: parametric neural cancellation during speech in auditory cortex

When we speak, we provide ourselves with auditory speech input. Efficient monitoring of speech is often hypothesized to depend on matching the predicted sensory consequences from internal motor commands (forward model) with actual sensory feedback. In this paper we tested the forward model hypothesis using functional Magnetic Resonance Imaging. We administered an overt picture naming task in which we parametrically reduced the quality of verbal feedback by noise masking. Presentation of the same auditory input in the absence of overt speech served as listening control condition. Our results suggest that a match between predicted and actual sensory feedback results in inhibition of cancellation of auditory activity because speaking with normal unmasked feedback reduced activity in the auditory cortex compared to listening control conditions. Moreover, during self-generated speech, activation in auditory cortex increased as the feedback quality of the self-generated speech decreased. We conclude that during speaking early auditory cortex is involved in matching external signals with an internally generated model or prediction of sensory consequences, the locus of which may reside in auditory or higher order brain areas. Matching at early auditory cortex may provide a very sensitive monitoring mechanism that highlights speech production errors at very early levels of processing and may efficiently determine the self-agency of speech input.     

An immunocytochemical mapping of somatostatin in the cat auditory cortex

Using an indirect immunoperoxidase technique, the localization of somatostatin-28 (1-12)-like immunoreactive fibers and cell bodies in the auditory cortex of the cat (anterior, primary, secondary, temporal, ventral, ventroposterior, posterior and dorsoposterior auditory fields) was studied. In general, the distribution of SOM-ir structures is widespread in the auditory cortex of the feline. A high density of immunoreactive fibers as well as a low density of cell bodies containing somatostatin were observed in all the layers of the eight above-mentioned auditory fields. These data indicate that somatostatin-28 (1-12) could act as a neurotransmitter and/or a neuromodulator in the auditory cortex of the cat. The origin of the SOM-ir fibers in the auditory cortex of the cat, as well as the issue of whether the cell bodies containing somatostatin-28 (1-12) are local or projecting neurons is discussed.     

Degraded auditory processing in a rat model of autism limits the speech representation in non‐primary auditory cortex

Although individuals with autism are known to have significant communication problems, the cellular mechanisms responsible for impaired communication are poorly understood. Valproic acid (VPA) is an anticonvulsant that is a known risk factor for autism in prenatally exposed children. Prenatal VPA exposure in rats causes numerous neural and behavioral abnormalities that mimic autism. We predicted that VPA exposure may lead to auditory processing impairments which may contribute to the deficits in communication observed in individuals with autism. In this study, we document auditory cortex responses in rats prenatally exposed to VPA. We recorded local field potentials and multiunit responses to speech sounds in primary auditory cortex, anterior auditory field, ventral auditory field. and posterior auditory field in VPA exposed and control rats. Prenatal VPA exposure severely degrades the precise spatiotemporal patterns evoked by speech sounds in secondary, but not primary auditory cortex. This result parallels findings in humans and suggests that secondary auditory fields may be more sensitive to environmental disturbances and may provide insight into possible mechanisms related to auditory deficits in individuals with autism. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 74: 972–986, 2014     

Processing of complex stimuli and natural scenes in the auditory cortex

Neuronal responses in auditory cortex show a fascinating mixture of characteristics that span the range from almost perfect copies of physical aspects of the stimuli to extremely complex context-dependent responses. Fast, highly stimulus-specific adaptation and slower plastic mechanisms work together to constantly adjust neuronal response properties to the statistics of the auditory scene. Evidence with converging implications suggests that the neuronal activity in primary auditory cortex represents sounds in terms of auditory objects rather than in terms of invariant acoustic features.     

豚鼠听觉诱发电位中潜伏期反应Pa波起源的研究

将豚鼠大脑皮层划分为五个区,采用大脑皮层吸除破坏与海人酸局部浸润破坏相结合的方法,研究了MLR的起源以及皮层各区域与MLR的关系。结果表明,破坏听区以外各区域,对MLR影响不大,一旦破坏听区皮层,MLR主波Pa立即消失,并且不再恢复。海人酸局部浸润破坏不仅进一步证明Pa波来源于听区皮层,而且还表明Pa波主要来源于听区皮层内神经无电活动,与皮层下听觉中枢及其向听区皮层投射的纤维无关。     

Dissociation of Detection and Discrimination of Pure Tones following Bilateral Lesions of Auditory Cortex

It is well known that damage to the peripheral auditory system causes deficits in tone detection as well as pitch and loudness perception across a wide range of frequencies. However, the extent to which to which the auditory cortex plays a critical role in these basic aspects of spectral processing, especially with regard to speech, music, and environmental sound perception, remains unclear. Recent experiments indicate that primary auditory cortex is necessary for the normally-high perceptual acuity exhibited by humans in pure-tone frequency discrimination. The present study assessed whether the auditory cortex plays a similar role in the intensity domain and contrasted its contribution to sensory versus discriminative aspects of intensity processing. We measured intensity thresholds for pure-tone detection and pure-tone loudness discrimination in a population of healthy adults and a middle-aged man with complete or near-complete lesions of the auditory cortex bilaterally. Detection thresholds in his left and right ears were 16 and 7 dB HL, respectively, within clinically-defined normal limits. In contrast, the intensity threshold for monaural loudness discrimination at 1 kHz was 6.5±2.1 dB in the left ear and 6.5±1.9 dB in the right ear at 40 dB sensation level, well above the means of the control population (left ear: 1.6±0.22 dB; right ear: 1.7±0.19 dB). The results indicate that auditory cortex lowers just-noticeable differences for loudness discrimination by approximately 5 dB but is not necessary for tone detection in quiet. Previous human and Old-world monkey experiments employing lesion-effect, neurophysiology, and neuroimaging methods to investigate the role of auditory cortex in intensity processing are reviewed.     

Progressive plasticity of auditory cortex during appetitive operant conditioning

In stimulus-response-outcome learning, different regions in the cortico-basal ganglia network are progressively involved according to the stage of learning. However, the involvement of sensory cortex remains ellusive even though massive cortical projections to the striatum imply its significant role in this learning. Here we show that the global tonotopic representation in the auditory cortex changed progressively depending on the stage of training in auditory operant conditioning. At the early stage, tone-responsive areas mainly in the core cortex expanded, while both the core and belt cortices shrank at the late stage as behavior became conditioned. Taken together with previous findings, this progressive global plasticity from the core to belt cortices suggests differentiated roles in these areas: the core cortex serves as a filter to better identify auditory objects for hierarchical computation within the belt cortex, while the belt stores auditory objects and affects decision making through direct projections to limbic system and higher association cortex. Thus, the progressive plasticity in the present study reflects a shift from identification to storage of a behaviorally relevant auditory object, which is potentially associated with a habitual behavior.     

Cortical representations of pitch in monkeys and humans

Pitch perception is crucial for vocal communication, music perception, and auditory object processing in a complex acoustic environment. How pitch is represented in the cerebral cortex has for a long time remained an unanswered question in auditory neuroscience. Several lines of evidence now point to a distinct non-primary region of auditory cortex in primates that contains a cortical representation of pitch.     

Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex

Besides the intensity and frequency of an auditory stimulus, the length of time that precedes the stimulation is an important factor that determines the magnitude of early evoked neural responses in the auditory cortex. Here we used chinchillas to demonstrate that the length of the silent period before the presentation of an auditory stimulus is a critical factor that modifies late oscillatory responses in the auditory cortex. We used tetrodes to record local-field potential (LFP) signals from the left auditory cortex of ten animals while they were stimulated with clicks, tones or noise bursts delivered at different rates and intensity levels. We found that the incidence of oscillatory activity in the auditory cortex of anesthetized chinchillas is dependent on the period of silence before stimulation and on the intensity of the auditory stimulus. In 62.5% of the recordings sites we found stimulus-related oscillations at around 8-20 Hz. Stimulus-induced oscillations were largest and consistent when stimuli were preceded by 5 s of silence and they were absent when preceded by less than 500 ms of silence. These results demonstrate that the period of silence preceding the stimulus presentation and the stimulus intensity are critical factors for the presence of these oscillations.     

Speech Rhythms and Multiplexed Oscillatory Sensory Coding in the Human Brain

Cortical oscillations are likely candidates for segmentation and coding of continuous speech. Here, we monitored continuous speech processing with magnetoencephalography (MEG) to unravel the principles of speech segmentation and coding. We demonstrate that speech entrains the phase of low-frequency (delta, theta) and the amplitude of high-frequency (gamma) oscillations in the auditory cortex. Phase entrainment is stronger in the right and amplitude entrainment is stronger in the left auditory cortex. Furthermore, edges in the speech envelope phase reset auditory cortex oscillations thereby enhancing their entrainment to speech. This mechanism adapts to the changing physical features of the speech envelope and enables efficient, stimulus-specific speech sampling. Finally, we show that within the auditory cortex, coupling between delta, theta, and gamma oscillations increases following speech edges. Importantly, all couplings (i.e., brain-speech and also within the cortex) attenuate for backward-presented speech, suggesting top-down control. We conclude that segmentation and coding of speech relies on a nested hierarchy of entrained cortical oscillations.     

Octave ratio as the absolute measurement unit of sensory communication in the cerebral cortex

The evidence for tonotopic representation in the auditory cortex, when a signal of the form δ?.δt= a constant is used, implies that frequency definition is in terms of octaves, and that “octavetopic” representation upon the auditory cortex should, and does, take place. A theoretical approximation of the evoked potential can be obtained from Laplace's equation in electromagnetic theory, which approaches an “octavetopic” representation. Thus, the empirical evidence already obtained for octave representation upon the auditory cortex is given a theoretical context.     

Effects of L-dopa during Auditory Instrumental Learning in Humans

The dopaminergic neurotransmitter system is critically involved in promoting plasticity in auditory cortex. We combined functional magnetic resonance imaging (fMRI) and a pharmacological manipulation to investigate dopaminergic modulation of neural activity in auditory cortex during instrumental learning. Volunteers either received 100 mg L-dopa (Madopar) or placebo in an appetitive, differential instrumental conditioning paradigm, which involved learning that a specific category of frequency modulated tones predicts a monetary reward when fast responses were made in a subsequent reaction time task. The other category of frequency modulated tones was not related to a reward. Our behavioral data provides evidence that dopaminergic stimulation differentially impacts on the speed of instrumental responding in rewarded and unrewarded trials. L-dopa increased neural BOLD activity in left auditory cortex to tones in rewarded and unrewarded trials. This increase was related to plasma L-dopa levels and learning rate. Our data thus provides evidence for dopaminergic modulation of neural activity in auditory cortex, which occurs for both auditory stimuli related to a later reward and those not related to a reward.