Activity In Auditory Regions Research Articles

Brain-wide circuitry underlying altered auditory habituation in zebrafish models of autism.

Auditory processing is widely understood to occur differently in autism, though the patterns of brain activity underlying these differences are not well understood. The diversity of autism also means brain-wide networks may change in various ways to produce similar behavioral outputs. We used larval zebrafish to investigate auditory habituation in four genetic lines relevant to autism: fmr1, mecp2, scn1lab and cntnap2. In free-swimming behavioral tests, we found each line had a unique profile of auditory hypersensitivity and/or delayed habituation. Combining the optical transparency of larval zebrafish with genetically encoded calcium indicators and light-sheet microscopy, we then observed brain-wide activity at cellular resolution during auditory habituation. As with behavior, each line showed unique alterations in brain-wide spontaneous activity, auditory processing, and adaptation in response to repetitive acoustic stimuli. We also observed commonalities in activity across our genetic lines that indicate shared circuit changes underlying certain aspects of their behavioral phenotypes. These were predominantly in regions involved in sensory integration and sensorimotor gating rather than primary auditory areas. Overlapping phenotypes include differences in the activity and functional connectivity of the telencephalon, thalamus, dopaminergic regions, and the locus coeruleus, and excitatory/inhibitory imbalance in the cerebellum. Unique phenotypes include loss of activity in the habenula in scn1lab, increased activity in auditory regions in fmr1, and differences in network activity over time in mecp2 and cntnap2. Comparing these distinct but overlapping brain-wide auditory networks furthers our understanding of how diverse genetic factors can produce similar behavioral effects through a range of circuit- and network-scale mechanisms.

On the speech envelope in the cortical tracking of speech

The synchronization between the speech envelope and neural activity in auditory regions, referred to as cortical tracking of speech (CTS), plays a key role in speech processing. The method selected for extracting the envelope is a crucial step in CTS measurement, and the absence of a consensus on best practices among the various methods can influence analysis outcomes and interpretation. Here, we systematically compare five standard envelope extraction methods the absolute value of Hilbert transform (absHilbert), gammatone filterbanks, heuristic approach, Bark scale, and vocalic energy), analyzing their impact on the CTS. We present performance metrics for each method based on the recording of brain activity from participants listening to speech in clear and noisy conditions, utilizing intracranial EEG, MEG and EEG data. As expected, we observed significant CTS in temporal brain regions below 10 Hz across all datasets, regardless of the extraction methods. In general, the gammatone filterbanks approach consistently demonstrated superior performance compared to other methods. Results from our study can guide scientists in the field to make informed decisions about the optimal analysis to extract the CTS, contributing to advancing the understanding of the neuronal mechanisms implicated in CTS.

Adaptation to mis-pronounced speech: evidence for a prefrontal-cortex repair mechanism

Speech is a complex and ambiguous acoustic signal that varies significantly within and across speakers. Despite the processing challenge that such variability poses, humans adapt to systematic variations in pronunciation rapidly. The goal of this study is to uncover the neurobiological bases of the attunement process that enables such fluent comprehension. Twenty-four native English participants listened to words spoken by a “canonical” American speaker and two non-canonical speakers, and performed a word-picture matching task, while magnetoencephalography was recorded. Non-canonical speech was created by including systematic phonological substitutions within the word (e.g. [s] → [sh]). Activity in the auditory cortex (superior temporal gyrus) was greater in response to substituted phonemes, and, critically, this was not attenuated by exposure. By contrast, prefrontal regions showed an interaction between the presence of a substitution and the amount of exposure: activity decreased for canonical speech over time, whereas responses to non-canonical speech remained consistently elevated. Grainger causality analyses further revealed that prefrontal responses serve to modulate activity in auditory regions, suggesting the recruitment of top-down processing to decode non-canonical pronunciations. In sum, our results suggest that the behavioural deficit in processing mispronounced phonemes may be due to a disruption to the typical exchange of information between the prefrontal and auditory cortices as observed for canonical speech.

Arterial spin labeling brain MRI study to evaluate the impact of deafness on cerebral perfusion in 79 children before cochlear implantation

Age at implantation is considered to be a major factor, influencing outcomes after pediatric cochlear implantation. In the absence of acoustic input, it has been proposed that cross-modal reorganization can be detrimental for adaptation to the new electrical input provided by a cochlear implant. Here, through a retrospective study, we aimed to investigate differences in cerebral blood flow (CBF) at rest prior to implantation in children with congenital deafness compared to normally hearing children. In addition, we looked at the putative link between pre-operative rest-CBF and the oral intelligibility scores at 12 months post-implantation. Finally, we observed the evolution of perfusion with age, within brain areas showing abnormal rest-CBF associated to deafness, in deaf children and in normally hearing children. In children older than 5 years old, results showed a significant bilateral hypoperfusion in temporal regions in deaf children, particularly in Heschl’s gyrus, and a significant hyperperfusion of occipital regions. Furthermore, in children older than 5 years old, whole brain voxel-by-voxel correlation analysis between pre-operative rest-CBF and oral intelligibility scores at 12 months post-implantation, showed significant negative correlation localized in the occipital regions: children who performed worse in the speech perception test one year after implantation were those presenting higher preoperative CBF values in these occipital regions. Finally, when comparing mean relative perfusion (extracted from the temporal regions found abnormal on whole-brain voxel-based analysis) across ages in patients and controls, we observed that the temporal perfusion evolution was significantly different in deaf children than in normally hearing children. Indeed, while temporal perfusion increased with age in normally hearing children, it remained stable in deaf children. We showed a critical period around 4 years old, where in the context of auditory deprivation, there is a lack of synaptic activity in auditory regions. These results support the benefits of early cochlear implantation to maximize the effectiveness of auditory rehabilitation and to avoid cross-modal reorganization.

Protecting memory from misinformation: Warnings modulate cortical reinstatement during memory retrieval

Exposure to even subtle forms of misleading information can significantly alter memory for past events. Memory distortion due to misinformation has been linked to faulty reconstructive processes during memory retrieval and the reactivation of brain regions involved in the initial encoding of misleading details (cortical reinstatement). The current study investigated whether warning participants about the threat of misinformation can modulate cortical reinstatement during memory retrieval and reduce misinformation errors. Participants watched a silent video depicting a crime (original event) and were given an initial test of memory for the crime details. Then, participants listened to an auditory narrative describing the crime in which some original details were altered (misinformation). Importantly, participants who received a warning about the reliability of the auditory narrative either before or after exposure to misinformation demonstrated less susceptibility to misinformation on a final test of memory compared to unwarned participants. Warned and unwarned participants also demonstrated striking differences in neural activity during the final memory test. Compared to participants who did not receive a warning, participants who received a warning (regardless of its timing) demonstrated increased activity in visual regions associated with the original source of information as well as decreased activity in auditory regions associated with the misleading source of information. Stronger visual reactivation was associated with reduced susceptibility to misinformation, whereas stronger auditory reactivation was associated with increased susceptibility to misinformation. Together, these results suggest that a simple warning can modulate reconstructive processes during memory retrieval and reduce memory errors due to misinformation.

Bilateral brain activity in auditory regions is necessary for successful vocal learning in songbirds

In humans and songbirds, neuronal activation for language and song shifts from bilateral- or diffuse-activation to left-hemispheric dominance while proficiency increases. Further parallels exist at the behavioural level: unstructured juvenile vocalizations become highly stereotyped adult vocalizations through a process of trial and error learning. Greater left-hemispheric dominance in the songbird caudomedial Nidopallium (NCM), a Wernicke-like region, is related to better imitation of the tutor’s song learned early in development, indicating a role for the left NCM in forming auditory memories. Here, we hypothesize that inhibition of the left NCM during interaction with a song tutor would impair imitation of the tutor’s song more than inhibition of the right NCM. We infused a transient sodium channel blocker (TTX) immediately prior to tutoring sessions in either the left or right auditory lobule of previously isolated juvenile male zebra finches (Taeniopygia guttata). Upon maturation, both right-infused and left-infused birds' tutor song imitation was significantly impaired. Left-infused birds also showed less consistency in the rhythmic stability of their song as well as increased pitch, suggesting a subtle division of function between the left and right auditory lobules.

Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

Low‐ and high‐frequency cortical oscillations play an important role in speech processing. Low‐frequency neural oscillations in the delta (<4 Hz) and theta (4–8 Hz) bands entrain to the prosodic and syllabic rates of speech, respectively. Theta band neural oscillations modulate high‐frequency neural oscillations in the gamma band (28−40 Hz), which have been hypothesized to be crucial for processing phonemes in natural speech. Since speech rate is known to vary considerably, both between and within talkers, it has yet to be determined whether this nested gamma response reflects an externally induced rhythm sensitive to the rate of the fine‐grained structure of the input or a speech rate−independent endogenous response. Here, we recorded magnetoencephalography responses from participants listening to a speech delivered at different rates: decelerated, normal, and accelerated. We found that the phase of theta band oscillations in left and right auditory regions adjusts to speech rate variations. Importantly, we showed that the peak of the gamma response—coupled to the phase of theta—follows the speech rate. This indicates that gamma activity in auditory regions synchronizes with the fine‐grain properties of speech, possibly reflecting detailed acoustic analysis of the input.

Task relevance modulates the behavioural and neural effects of sensory predictions.

The brain is thought to generate internal predictions to optimize behaviour. However, it is unclear whether predictions signalling is an automatic brain function or depends on task demands. Here, we manipulated the spatial/temporal predictability of visual targets, and the relevance of spatial/temporal information provided by auditory cues. We used magnetoencephalography (MEG) to measure participants’ brain activity during task performance. Task relevance modulated the influence of predictions on behaviour: spatial/temporal predictability improved spatial/temporal discrimination accuracy, but not vice versa. To explain these effects, we used behavioural responses to estimate subjective predictions under an ideal-observer model. Model-based time-series of predictions and prediction errors (PEs) were associated with dissociable neural responses: predictions correlated with cue-induced beta-band activity in auditory regions and alpha-band activity in visual regions, while stimulus-bound PEs correlated with gamma-band activity in posterior regions. Crucially, task relevance modulated these spectral correlates, suggesting that current goals influence PE and prediction signalling.

Whispering - The hidden side of auditory communication

Whispering is a unique expression mode that is specific to auditory communication. Individuals switch their vocalization mode to whispering especially when affected by inner emotions in certain social contexts, such as in intimate relationships or intimidating social interactions. Although this context-dependent whispering is adaptive, whispered voices are acoustically far less rich than phonated voices and thus impose higher hearing and neural auditory decoding demands for recognizing their socio-affective value by listeners. The neural dynamics underlying this recognition especially from whispered voices are largely unknown. Here we show that whispered voices in humans are considerably impoverished as quantified by an entropy measure of spectral acoustic information, and this missing information needs large-scale neural compensation in terms of auditory and cognitive processing. Notably, recognizing the socio-affective information from voices was slightly more difficult from whispered voices, probably based on missing tonal information. While phonated voices elicited extended activity in auditory regions for decoding of relevant tonal and time information and the valence of voices, whispered voices elicited activity in a complex auditory-frontal brain network. Our data suggest that a large-scale multidirectional brain network compensates for the impoverished sound quality of socially meaningful environmental signals to support their accurate recognition and valence attribution.

Male song quality modulates c-Fos expression in the auditory forebrain of the female canary

In canaries, specific phrases of male song (sexy songs, SS) that are difficult to produce are especially attractive for females. Females exposed to SS produce more copulation displays and deposit more testosterone into their eggs than females exposed to non-sexy songs (NS). Increased expression of the immediate early genes c-Fos or zenk (a.k.a. egr-1) has been observed in the auditory forebrain of female songbirds hearing attractive songs. C-Fos immunoreactive (Fos-ir) cell numbers were quantified here in the brain of female canaries that had been collected 30min after they had been exposed for 60min to the playback of SS or NS or control white noise. Fos-ir cell numbers increased in the caudomedial mesopallium (CMM) and caudomedial nidopallium (NCM) of SS birds as compared to controls. Song playback (pooled SS and NS) also tended to increase average Fos-ir cell numbers in the mediobasal hypothalamus (MBH) but this effect did not reach full statistical significance. At the individual level, Fos expression in CMM was correlated with its expression in NCM and in MBH but also with the frequency of calls that females produced in response to the playbacks. These data thus indicate that male songs of different qualities induce a differential metabolic activation of NCM and CMM. The correlation between activation of auditory regions and of the MBH might reflect the link between auditory stimulation and changes in behavior and reproductive physiology.

Glutamic acid decarboxylase levels in the cochlear nucleus of rats with acoustic trauma-induced chronic tinnitus

Tinnitus is the perception of phantom sounds, a phenomenon believed to be due to abnormal neuronal activity in auditory regions of the CNS such as the brainstem cochlear nucleus (CN). One possible mechanism for the abnormal neuronal activity in the CN, supported by recent animal studies, is a decrease in GABAergic inhibition. One possible explanation for this is a decrease in the enzyme responsible for the synthesis of GABA, glutamic acid decarboxylase (GAD). In this study, we used immunohistochemistry to analyse the levels of GAD in the dorsal and ventral CN of rats that had been exposed to noise trauma and had been confirmed to exhibit psychophysical evidence of tinnitus (at 17.5 weeks post-exposure) using a conditioned behavioural task. At 22 weeks following noise trauma or sham treatment, the levels of GAD in the dorsal and ventral CN were not significantly different. This result suggests that acoustic trauma that can cause chronic tinnitus is not associated with changes in GAD in the CN at 22 weeks post-exposure.

Auditory–Motor Interactions for the Production of Native and Non-Native Speech

During speech production, auditory processing of self-generated speech is used to adjust subsequent articulations. The current study investigated how the proposed auditory-motor interactions are manifest at the neural level in native and non-native speakers of English who were overtly naming pictures of objects and reading their written names. Data were acquired with functional magnetic resonance imaging and analyzed with dynamic causal modeling. We found that (1) higher activity in articulatory regions caused activity in auditory regions to decrease (i.e., auditory suppression), and (2) higher activity in auditory regions caused activity in articulatory regions to increase (i.e., auditory feedback). In addition, we were able to demonstrate that (3) speaking in a non-native language involves more auditory feedback and less auditory suppression than speaking in a native language. The difference between native and non-native speakers was further supported by finding that, within non-native speakers, there was less auditory feedback for those with better verbal fluency. Consequently, the networks of more fluent non-native speakers looked more like those of native speakers. Together, these findings provide a foundation on which to explore auditory-motor interactions during speech production in other human populations, particularly those with speech difficulties.

Modulation of Auditory Cortex Response to Pitch Variation Following Training with Microtonal Melodies

We tested changes in cortical functional response to auditory patterns in a configural learning paradigm. We trained 10 human listeners to discriminate micromelodies (consisting of smaller pitch intervals than normally used in Western music) and measured covariation in blood oxygenation signal to increasing pitch interval size in order to dissociate global changes in activity from those specifically associated with the stimulus feature that was trained. A psychophysical staircase procedure with feedback was used for training over a 2-week period. Behavioral tests of discrimination ability performed before and after training showed significant learning on the trained stimuli, and generalization to other frequencies and tasks; no learning occurred in an untrained control group. Before training the functional MRI data showed the expected systematic increase in activity in auditory cortices as a function of increasing micromelody pitch interval size. This function became shallower after training, with the maximal change observed in the right posterior auditory cortex. Global decreases in activity in auditory regions, along with global increases in frontal cortices also occurred after training. Individual variation in learning rate was related to the hemodynamic slope to pitch interval size, such that those who had a higher sensitivity to pitch interval variation prior to learning achieved the fastest learning. We conclude that configural auditory learning entails modulation in the response of auditory cortex to the trained stimulus feature. Reduction in blood oxygenation response to increasing pitch interval size suggests that fewer computational resources, and hence lower neural recruitment, is associated with learning, in accord with models of auditory cortex function, and with data from other modalities.

Functional Brain Network Characterization and Adaptivity during Task Practice in Healthy Volunteers and People with Schizophrenia1

Cognitive remediation involves task practice and may improve deficits in people suffering from schizophrenia, but little is known about underlying neurophysiological mechanisms. In people with schizophrenia and controls, we used magnetoencephalography (MEG) to examine accuracy and practice-related changes in parameters indexing neural network structure and activity, to determine whether these might be useful assays of the efficacy of cognitive remediation. Two MEG recordings were acquired during performance of a tone discrimination task used to improve the acuity of auditory processing, before and after ∼2.5 h of task practice. Accuracy before practice was negatively correlated with beta-band cost efficiency, a graph theoretical measure of network organization. Synthetic aperture magnetometry was used to localize brain oscillations with high spatial accuracy; results demonstrated sound and sensorimotor modulations of the beta band in temporo-parietal regions and the sensorimotor cortex respectively. High-gamma activity also correlated with sensorimotor processing during the task, with activation of auditory regions following sound stimulation, and activation of the left sensorimotor cortex preceding the button press. High-gamma power in the left frontal cortex was also found to correlate with accuracy. Following practice, sound-induced broad-band power in the left angular gyri increased. Accuracy improved and was found to correlate with increased mutual information (MI) between sensors in temporal–parietal regions in the beta band but not global cost efficiency. Based on these results, we conclude that hours of task practice can induce meso-scale changes such as increased power in relevant brain regions as well as changes in MI that correlate with improved accuracy.

Congruence of happy and sad emotion in music and faces modifies cortical audiovisual activation

BackgroundThe powerful emotion inducing properties of music are well-known, yet music may convey differing emotional responses depending on environmental factors. We hypothesized that neural mechanisms involved in listening to music may differ when presented together with visual stimuli that conveyed the same emotion as the music when compared to visual stimuli with incongruent emotional content. MethodsWe designed this study to determine the effect of auditory (happy and sad instrumental music) and visual stimuli (happy and sad faces) congruent or incongruent for emotional content on audiovisual processing using fMRI blood oxygenation level-dependent (BOLD) signal contrast. The experiment was conducted in the context of a conventional block-design experiment. A block consisted of three emotional ON periods, music alone (happy or sad music), face alone (happy or sad faces), and music combined with faces where the music excerpt was played while presenting either congruent emotional faces or incongruent emotional faces. ResultsWe found activity in the superior temporal gyrus (STG) and fusiform gyrus (FG) to be differentially modulated by music and faces depending on the congruence of emotional content. There was a greater BOLD response in STG when the emotion signaled by the music and faces was congruent. Furthermore, the magnitude of these changes differed for happy congruence and sad congruence, i.e., the activation of STG when happy music was presented with happy faces was greater than the activation seen when sad music was presented with sad faces. In contrast, incongruent stimuli diminished the BOLD response in STG and elicited greater signal change in bilateral FG. Behavioral testing supplemented these findings by showing that subject ratings of emotion in faces were influenced by emotion in music. When presented with happy music, happy faces were rated as more happy (p=0.051) and sad faces were rated as less sad (p=0.030). When presented with sad music, happy faces were rated as less happy (p=0.008) and sad faces were rated as sadder (p=0.002). InterpretationHappy–sad congruence across modalities may enhance activity in auditory regions while incongruence appears to impact the perception of visual affect, leading to increased activation in face processing regions such as the FG. We suggest that greater understanding of the neural bases of happy–sad congruence across modalities can shed light on basic mechanisms of affective perception and experience and may lead to novel insights in the study of emotion regulation and therapeutic use of music.