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ENeuro Jun 2024The zebrafish, a widely used model in neurobiology, relies on hearing in aquatic environments. Unfortunately, its auditory pathways have mainly been studied in larvae....
The zebrafish, a widely used model in neurobiology, relies on hearing in aquatic environments. Unfortunately, its auditory pathways have mainly been studied in larvae. In this study, we examined the involvement of the anterior tuberal nucleus (AT) in auditory processing in adult zebrafish. Our tract-tracing experiments revealed that the dorsal subdivision of AT is strongly bidirectionally connected to the central nucleus of the torus semicircularis (TSc), a major auditory nucleus in fishes. Immunohistochemical visualisation of the ribosomal protein S6 (pS6) phosphorylation to map neural activity in response to auditory stimulation substantiated this finding: the dorsal but not the ventral part of AT responded strongly to auditory stimulation. A similar response to auditory stimulation was present in the TSc but not in the nucleus isthmi (NI), a visual region, which we used as a control for testing if the pS6 activation was specific to the auditory stimulation. We also measured the time course of pS6 phosphorylation, which was previously unreported in teleost fish. After auditory stimulation, we found that pS6 phosphorylation peaked between 100-130 minutes and returned to baseline levels after 190 minutes. This information will be valuable for the design of future pS6 experiments. Our results suggest an anatomical and functional subdivision of AT, where only the dorsal part connects to the auditory network and processes auditory information. We investigated the involvement of the anterior tuberal nucleus in zebrafish in auditory processing. Our study revealed a functional and anatomical subdivision of this region. We show that its dorsal subdivision is strongly connected to the central nucleus of the torus semicircularis, a major auditory nucleus in fishes. pS6 phosphorylation, as an indirect marker of neuronal activity after auditory stimulation, substantiated that only the dorsal anterior tuberal nucleus, processes auditory information. We also show that after auditory stimulation, pS6 phosphorylation peaked between 100-130 minutes and returned to baseline levels after 190 minutes, providing valuable information for future studies.
PubMed: 38918052
DOI: 10.1523/ENEURO.0062-24.2024 -
BioRxiv : the Preprint Server For... Jun 2024Auditory perception is established through experience-dependent stimuli exposure during sensitive developmental periods; however, little is known regarding the...
Auditory perception is established through experience-dependent stimuli exposure during sensitive developmental periods; however, little is known regarding the structural development of the central auditory pathway in humans. The present study characterized the regional developmental trajectories of the ascending auditory pathway from the brainstem to the auditory cortex from infancy through adolescence using a novel diffusion MRI-based tractography approach and along-tract analyses. We used diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) to quantify the magnitude and timing of auditory pathway microstructural maturation. We found spatially varying patterns of white matter maturation along the length of the tract, with inferior brainstem regions developing earlier than thalamocortical projections and left hemisphere tracts developing earlier than the right. These results help to characterize the processes that give rise to functional auditory processing and may provide a baseline for detecting abnormal development.
PubMed: 38915661
DOI: 10.1101/2024.06.10.597798 -
Noise & HealthDue to the abnormal structure and function of brain neural networks in special populations, such as children, elderly individuals, and individuals with mental disorders,... (Review)
Review
Due to the abnormal structure and function of brain neural networks in special populations, such as children, elderly individuals, and individuals with mental disorders, noise exposure is more likely to have negative psychological and cognitive nonauditory effects on these individuals. There are unique and complex neural mechanisms underlying this phenomenon. For individuals with mental disorders, there are anomalies such as structural atrophy and decreased functional activation in brain regions involved in emotion and cognitive processing, such as the prefrontal cortex (PFC). Noise exposure can worsen these abnormalities in relevant brain regions, further damaging neural plasticity and disrupting normal connections and the transmission of information between the PFC and other brain areas by causing neurotransmitter imbalances. In the case of children, in a noisy environment, brain regions such as the left inferior frontal gyrus and PFC, which are involved in growth and development, are more susceptible to structural and functional changes, leading to neurodegenerative alterations. Furthermore, noise exposure can interrupt auditory processing neural pathways or impair inhibitory functions, thus hindering children's ability to map sound to meaning in neural processes. For elderly people, age-related shrinkage of brain regions such as the PFC, as well as deficiencies in hormone, neurotransmitter, and nutrient levels, weakens their ability to cope with noise. Currently, it is feasible to propose and apply coping strategies to improve the nonauditory effects of noise exposure on special populations based on the plasticity of the human brain.
Topics: Humans; Noise; Child; Brain; Aged; Neuronal Plasticity; Environmental Exposure; Prefrontal Cortex; Mental Disorders
PubMed: 38904804
DOI: 10.4103/nah.nah_78_23 -
Journal of the Royal Society, Interface Jun 2024Many animals employ a second frequency filter beyond the initial filtering of the eardrum (or tympanal membrane). In the field cricket ear, both the filtering mechanism...
Coupled membranes: a mechanism of frequency filtering and transmission in the field cricket ear evidenced by micro-computed tomography, laser Doppler vibrometry and finite element analysis.
Many animals employ a second frequency filter beyond the initial filtering of the eardrum (or tympanal membrane). In the field cricket ear, both the filtering mechanism and the transmission path from the posterior tympanal membrane (PTM) have remained unclear. A mismatch between PTM vibrations and sensilla tuning has prompted speculations of a second filter. PTM coupling to the tracheal branches is suggested to support a transmission pathway. Here, we present three independent lines of evidence converging on the same conclusion: the existence of a series of linked membranes with distinct resonant frequencies serving both filtering and transmission functions. Micro-computed tomography (µ-CT) highlighted the 'dividing membrane (DivM)', separating the tracheal branches and connected to the PTM via the dorsal membrane of the posterior tracheal branch (DM-PTB). Thickness analysis showed the DivM to share significant thinness similarity with the PTM. Laser Doppler vibrometry indicated the first of two PTM vibrational peaks, at 6 and 14 kHz, originates not from the PTM but from the coupled DM-PTB. This result was corroborated by µ-CT-based finite element analysis. These findings clarify further the biophysical source of neuroethological pathways in what is an important model of behavioural neuroscience. Tuned microscale coupled membranes may also hold biomimetic relevance.
Topics: Animals; Gryllidae; X-Ray Microtomography; Finite Element Analysis; Tympanic Membrane; Vibration
PubMed: 38903010
DOI: 10.1098/rsif.2023.0779 -
Behavioral and Brain Functions : BBF Jun 2024The Default Mode Network (DMN) is a central neural network, with recent evidence indicating that it is composed of functionally distinct sub-networks. Methylphenidate... (Randomized Controlled Trial)
Randomized Controlled Trial
BACKGROUND
The Default Mode Network (DMN) is a central neural network, with recent evidence indicating that it is composed of functionally distinct sub-networks. Methylphenidate (MPH) administration has been shown before to modulate impulsive behavior, though it is not yet clear whether these effects relate to MPH-induced changes in DMN connectivity. To address this gap, we assessed the impact of MPH administration on functional connectivity patterns within and between distinct DMN sub-networks and tested putative relations to variability in sub-scales of impulsivity.
METHODS
Fifty-five right-handed healthy adults underwent two resting-state functional MRI (rs-fMRI) scans, following acute administration of either MPH (20 mg) or placebo, via a randomized double-blind placebo-controlled design. Graph modularity analysis was implemented to fractionate the DMN into distinct sub-networks based on the impact of MPH (vs. placebo) on DMN connectivity patterns with other neural networks.
RESULTS
MPH administration led to an overall decreased DMN connectivity, particularly with the auditory, cinguloopercular, and somatomotor networks, and increased connectivity with the parietomedial network. Graph analysis revealed that the DMN could be fractionated into two distinct sub-networks, with one exhibiting MPH-induced increased connectivity and the other decreased connectivity. Decreased connectivity of the DMN sub-network with the cinguloopercular network following MPH administration was associated with elevated impulsivity and non-planning impulsiveness.
CONCLUSION
Current findings highlight the intricate effects of MPH administration on DMN rs-fMRI connectivity, uncovering its opposing impact on distinct DMN sub-divisions. MPH-induced dynamics in DMN connectivity patterns with other neural networks may account for some of the effects of MPH administration on impulsive behavior.
Topics: Humans; Methylphenidate; Adult; Male; Magnetic Resonance Imaging; Female; Central Nervous System Stimulants; Default Mode Network; Young Adult; Double-Blind Method; Nerve Net; Impulsive Behavior; Connectome; Brain; Neural Pathways
PubMed: 38902791
DOI: 10.1186/s12993-024-00242-1 -
BioRxiv : the Preprint Server For... Jun 2024In school-age children, the myelination of the auditory radiation thalamocortical pathway is associated with the latency of auditory evoked responses, with the...
In school-age children, the myelination of the auditory radiation thalamocortical pathway is associated with the latency of auditory evoked responses, with the myelination of thalamocortical axons facilitating the rapid propagation of acoustic information. Little is known regarding this auditory system function-structure association in infants and toddlers. The present study tested the hypothesis that maturation of auditory radiation white-matter microstructure (e.g., fractional anisotropy (FA); measured using diffusion-weighted MRI) is associated with the latency of the infant auditory response (P2m measured using magnetoencephalography, MEG) in a cross-sectional (2 to 24 months) as well as longitudinal cohort (2 to 29 months) of typically developing infants and toddlers. In the cross-sectional sample, non-linear maturation of P2m latency and auditory radiation diffusion measures were observed. After removing the variance associated with age in both P2m latency and auditory radiation diffusion measures, auditory radiation still accounted for significant variance in P2m latency. In the longitudinal sample, latency and FA associations could be observed at the level of a single child. Findings provide strong support for a contribution of auditory radiation white matter to rapid cortical auditory encoding processes in infants.
PubMed: 38895425
DOI: 10.1101/2024.06.05.597426 -
BioRxiv : the Preprint Server For... Jun 2024Our sense of hearing is critically dependent on the spiral ganglion neurons (SGNs) that connect the sound receptors in the organ of Corti (OC) to the cochlear nuclei of...
Our sense of hearing is critically dependent on the spiral ganglion neurons (SGNs) that connect the sound receptors in the organ of Corti (OC) to the cochlear nuclei of the hindbrain. Type I SGNs innervate inner hair cells (IHCs) to transmit sound signals, while type II SGNs (SGNIIs) innervate outer hair cells (OHCs) to detect moderate-to-intense sound. During development, SGNII afferents make a characteristic 90-degree turn toward the base of the cochlea and innervate multiple OHCs. It has been shown that the Planar Cell Polarity (PCP) pathway acts non-autonomously to mediate environmental cues in the cochlear epithelium for SGNII afferent turning towards the base. However, the underlying mechanisms are unknown. Here, we present evidence that PCP signaling regulates multiple downstream effectors to influence cell adhesion and the cytoskeleton in cochlear supporting cells (SCs), which serve as intermediate targets of SGNII afferents. We show that the core PCP gene Vangl2 regulates the localization of the small GTPase Rac1 and the cell adhesion molecule Nectin3 at SC-SC junctions through which SGNII afferents travel. Through genetic analysis, we also show that loss of Rac1 or Nectin3 partially phenocopied SGNII peripheral afferent turning defects in mutants, and that Rac1 plays a non-autonomous role in this process in part by regulating PCP protein localization at the SC-SC junctions. Additionally, epistasis analysis indicates that Nectin3 and Rac1 likely act in the same genetic pathway to control SGNII afferent turning. Together, these experiments identify Nectin3 and Rac1 as novel regulators of PCP-directed SGNII axon guidance in the cochlea.
PubMed: 38895287
DOI: 10.1101/2024.06.05.597585 -
Journal of Clinical Medicine May 2024Progressive auditory dysfunction is common in patients with generalized neurodegenerative conditions, but clinicians currently lack the diagnostic tools to determine the...
BACKGROUND
Progressive auditory dysfunction is common in patients with generalized neurodegenerative conditions, but clinicians currently lack the diagnostic tools to determine the location/degree of the pathology and, hence, to provide appropriate intervention. In this study, we present the white-matter microstructure measurements derived from a novel diffusion-weighted magnetic resonance imaging (dMRI) technique in a patient with axonal auditory neuropathy and consider the findings in relation to the auditory intervention outcomes.
METHODS
We tracked the hearing changes in an adolescent with Riboflavin Transporter Deficiency (Type 2), evaluating the sound detection/discrimination, auditory evoked potentials, and both structural- and diffusion-weighted MRI findings over a 3-year period. In addition, we explored the effect of bilateral cochlear implantation in this individual.
RESULTS
Between the ages of 15 years and 18 years, the patient showed a complete loss of functional hearing ability. The auditory brainstem response testing indicated an auditory neuropathy with evidence of normal cochlear function but disrupted auditory neural activity. While three structural MRI assessments across this period showed a clinically normal cochleovestibular anatomy, the dMRI evaluation revealed a significant loss of fiber density consistent with axonopathy. The subsequent cochlear implant function was affected with the high levels of current required to elicit auditory sensations and concomitant vestibular and facial nerve stimulation issues.
CONCLUSIONS
The case study demonstrates the ability of dMRI technologies to identify the subtle white-matter microstructure changes in the auditory pathway, which may disrupt the neural function in patients with auditory axonopathy.
PubMed: 38892782
DOI: 10.3390/jcm13113072 -
Human Brain Mapping Jun 2024Is language distinct from other cognition during development? Does neural machinery for language emerge from general-purpose neural mechanisms, becoming tuned for...
Is language distinct from other cognition during development? Does neural machinery for language emerge from general-purpose neural mechanisms, becoming tuned for language after years of experience and maturation? Answering these questions will shed light on the origins of domain-specificity in the brain. We address these questions using precision fMRI, scanning young children (35 months to 9 years of age) on an auditory language localizer, spatial working memory localizer (engaging the domain-general multiple demand [MD] network), and a resting-state scan. We create subject-specific functional regions of interest for each network and examine their selectivity, specificity, and functional connectivity. We find young children show domain-specific, left-lateralized language activation, and that the language network is not responsive to domain-general cognitive load. Additionally, the cortically adjacent MD network is selective to cognitive load, but not to language. These networks show higher within versus between-network functional connectivity. This connectivity is stable across ages (examined cross-sectionally and longitudinally), whereas language responses increase with age and across time within subject, reflecting a domain-specific developmental change. Overall, we provide evidence for a double dissociation of the language and MD network throughout development, in both their function and connectivity. These findings suggest that domain-specificity, even for uniquely human cognition like language, develops early and distinctly from mechanisms that presumably support other human cognition.
Topics: Humans; Magnetic Resonance Imaging; Child; Male; Female; Child, Preschool; Language; Cognition; Brain; Brain Mapping; Memory, Short-Term; Child Development; Nerve Net; Neural Pathways; Longitudinal Studies; Language Development
PubMed: 38888027
DOI: 10.1002/hbm.26757 -
Frontiers in Synaptic Neuroscience 2024Age-related hearing difficulties have a complex etiology that includes degenerative processes in the sensory cochlea. The cochlea comprises the start of the afferent,...
INTRODUCTION
Age-related hearing difficulties have a complex etiology that includes degenerative processes in the sensory cochlea. The cochlea comprises the start of the afferent, ascending auditory pathway, but also receives efferent feedback innervation by two separate populations of brainstem neurons: the medial olivocochlear and lateral olivocochlear pathways, innervating the outer hair cells and auditory-nerve fibers synapsing on inner hair cells, respectively. Efferents are believed to improve hearing under difficult conditions, such as high background noise. Here, we compare olivocochlear efferent innervation density along the tonotopic axis in young-adult and aged gerbils (at ~50% of their maximum lifespan potential), a classic animal model for age-related hearing loss.
METHODS
Efferent synaptic terminals and sensory hair cells were labeled immunohistochemically with anti-synaptotagmin and anti-myosin VIIa, respectively. Numbers of hair cells, numbers of efferent terminals, and the efferent innervation area were quantified at seven tonotopic locations along the organ of Corti.
RESULTS
The tonotopic distribution of olivocochlear innervation in the gerbil was similar to that previously shown for other species, with a slight apical cochlear bias in presumed lateral olivocochlear innervation (inner-hair-cell region), and a broad mid-cochlear peak for presumed medial olivocochlear innervation (outer-hair-cell region). We found significant, age-related declines in overall efferent innervation to both the inner-hair-cell and the outer-hair-cell region. However, when accounting for the age-related losses in efferent target structures, the innervation density of surviving elements proved unchanged in the inner-hair-cell region. For outer hair cells, a pronounced increase of orphaned outer hair cells, i.e., lacking efferent innervation, was observed. Surviving outer hair cells that were still efferently innervated retained a nearly normal innervation.
DISCUSSION
A comparison across species suggests a basic aging scenario where outer hair cells, type-I afferents, and the efferents associated with them, steadily die away with advancing age, but leave the surviving cochlear circuitry largely intact until an advanced age, beyond 50% of a species' maximum lifespan potential. In the outer-hair-cell region, MOC degeneration may precede outer-hair-cell death, leaving a putatively transient population of orphaned outer hair cells that are no longer under efferent control.
PubMed: 38887655
DOI: 10.3389/fnsyn.2024.1422330