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Predictive coding and stochastic resonance as fundamental principles of auditory phantom perception.Brain : a Journal of Neurology Dec 2023Mechanistic insight is achieved only when experiments are employed to test formal or computational models. Furthermore, in analogy to lesion studies, phantom perception... (Review)
Review
Mechanistic insight is achieved only when experiments are employed to test formal or computational models. Furthermore, in analogy to lesion studies, phantom perception may serve as a vehicle to understand the fundamental processing principles underlying healthy auditory perception. With a special focus on tinnitus-as the prime example of auditory phantom perception-we review recent work at the intersection of artificial intelligence, psychology and neuroscience. In particular, we discuss why everyone with tinnitus suffers from (at least hidden) hearing loss, but not everyone with hearing loss suffers from tinnitus. We argue that intrinsic neural noise is generated and amplified along the auditory pathway as a compensatory mechanism to restore normal hearing based on adaptive stochastic resonance. The neural noise increase can then be misinterpreted as auditory input and perceived as tinnitus. This mechanism can be formalized in the Bayesian brain framework, where the percept (posterior) assimilates a prior prediction (brain's expectations) and likelihood (bottom-up neural signal). A higher mean and lower variance (i.e. enhanced precision) of the likelihood shifts the posterior, evincing a misinterpretation of sensory evidence, which may be further confounded by plastic changes in the brain that underwrite prior predictions. Hence, two fundamental processing principles provide the most explanatory power for the emergence of auditory phantom perceptions: predictive coding as a top-down and adaptive stochastic resonance as a complementary bottom-up mechanism. We conclude that both principles also play a crucial role in healthy auditory perception. Finally, in the context of neuroscience-inspired artificial intelligence, both processing principles may serve to improve contemporary machine learning techniques.
Topics: Humans; Tinnitus; Bayes Theorem; Artificial Intelligence; Auditory Perception; Hearing Loss; Auditory Pathways
PubMed: 37503725
DOI: 10.1093/brain/awad255 -
Journal of Comparative Physiology. A,... Jan 2023Albert Feng pioneered the study of neuroethology of sound localization in anurans by combining behavioral experiments on phonotaxis with detailed investigations of... (Review)
Review
Albert Feng pioneered the study of neuroethology of sound localization in anurans by combining behavioral experiments on phonotaxis with detailed investigations of neural processing of sound direction from the periphery to the central nervous system. The main advantage of these studies is that many species of female frogs readily perform phonotaxis towards loudspeakers emitting the species-specific advertisement call. Behavioral studies using synthetic calls can identify which parameters are important for phonotaxis and also quantify localization accuracy. Feng was the first to investigate binaural processing using single-unit recordings in the first two auditory nuclei in the central auditory pathway and later investigated the directional properties of auditory nerve fibers with free-field stimulation. These studies showed not only that the frog ear is inherently directional by virtue of acoustical coupling or crosstalk between the two eardrums, but also confirmed that there are extratympanic pathways that affect directionality in the low-frequency region of the frog's hearing range. Feng's recordings in the midbrain also showed that directional information is enhanced by cross-midline inhibition. An important contribution toward the end of his career involved his participation in neuroethological research with a team of scientists working with frogs that produce ultrasonic calls.
Topics: Female; Animals; Sound Localization; Hearing; Sound; Auditory Pathways; Anura; Acoustic Stimulation
PubMed: 36201014
DOI: 10.1007/s00359-022-01576-9 -
Neuroscience Letters Apr 2022The inferior colliculus (IC) is a critical hub of the central auditory system (CAS), and a majority of the ascending and descending auditory synapses converge in the IC.... (Review)
Review
The inferior colliculus (IC) is a critical hub of the central auditory system (CAS), and a majority of the ascending and descending auditory synapses converge in the IC. With considerable methodological advances in neural tract tracing techniques, one can clearly visualize various sub-compartments of the IC. Herein, we compared the inputs and outputs between the two sub-regions of the non-lemniscal IC, namely, the dorsal and external cortex of the IC. The non-lemniscal IC plays a crucial role in multisensory integration and animal behavior, and the dorsal and external regions are distinct in many aspects, including molecular expression and neural circuits. They may serve integration and regulation functions via parallel pathways. As previous studies have mostly treated these two parts as a whole, we suggest that the two sub-regions of the non-lemniscal IC should be studied separately in future IC functional investigations.
Topics: Animals; Auditory Pathways; Inferior Colliculi; Synapses
PubMed: 35271997
DOI: 10.1016/j.neulet.2022.136567 -
Der Ophthalmologe : Zeitschrift Der... Nov 2020
Topics: Auditory Pathways; Humans; Photic Stimulation; Visual Pathways; Visual Perception
PubMed: 33151435
DOI: 10.1007/s00347-020-01082-w -
Developmental Dynamics : An Official... Jan 2023Acoustic communication relies crucially on accurate interpretation of information about the intensity, frequency, timing, and location of diverse sound stimuli in the... (Review)
Review
Acoustic communication relies crucially on accurate interpretation of information about the intensity, frequency, timing, and location of diverse sound stimuli in the environment. To meet this demand, neurons along different levels of the auditory system form precisely organized neural circuits. The assembly of these precise circuits requires tight regulation and coordination of multiple developmental processes. Several groups of axon guidance molecules have proven critical in controlling these processes. Among them, the family of Eph receptors and their ephrin ligands emerge as one group of key players. They mediate diverse functions at multiple levels of the auditory pathway, including axon guidance and targeting, topographic map formation, as well as cell migration and tissue pattern formation. Here, we review our current knowledge of how Eph and ephrin molecules regulate different processes in the development and maturation of central auditory circuits.
Topics: Ephrins; Auditory Pathways; Neurons; Receptors, Eph Family; Signal Transduction
PubMed: 35705527
DOI: 10.1002/dvdy.506 -
PloS One 2021The aim of the present study is to show a MR procedure for the evaluation of simultaneous left and right auditory functions with functional MRI, and high-resolution...
PURPOSE
The aim of the present study is to show a MR procedure for the evaluation of simultaneous left and right auditory functions with functional MRI, and high-resolution acquisition of anatomical auditory pathway using parallel-transmit (pTx) methods at 7T.
METHODS
The time-efficient MR acquisition included two steps: RF weights were optimized for the regions-of-interest and high-resolution MR images of the inner-ear were acquired for the first 30 min (400 μm-iso resolution) followed by functional MRI acquisitions along the whole auditory pathway during the next 20 minutes. Data was processed with a linear cross-correlation analysis to define frequency preferences for each voxel in the auditory relays.
RESULTS
Tonotopic maps revealed ordered bilateral frequency gradients in the auditory relays whereas at the level of the cochlear nuclei and superior olivary complexes the frequency gradients were less evident. A 21% increase in transmit-field efficiency was achieved over the left/right inner-ear regions and thus its main structures were clearly discernible using the pTx methods, compared to a single transmit RF coil.
CONCLUSION
Using 7T pTx allows a fast (less than 60 min in total) and qualitative evaluation of the simultaneous left and right auditory response along the entire auditory pathway, together with high-resolution anatomical images of the inner-ear. This could be further used for patient examination at 7T.
Topics: Adult; Auditory Pathways; Ear, Inner; Equipment Design; Female; Humans; Image Processing, Computer-Assisted; Magnetic Resonance Imaging; Male; Young Adult
PubMed: 34492032
DOI: 10.1371/journal.pone.0254378 -
Hearing Research Feb 2024The inferior colliculus (IC) is a critical computational hub in the central auditory pathway. From its position in the midbrain, the IC receives nearly all the ascending... (Review)
Review
The inferior colliculus (IC) is a critical computational hub in the central auditory pathway. From its position in the midbrain, the IC receives nearly all the ascending output from the lower auditory brainstem and provides the main source of auditory information to the thalamocortical system. In addition to being a crossroads for auditory circuits, the IC is rich with local circuits and contains more than five times as many neurons as the nuclei of the lower auditory brainstem combined. These results hint at the enormous computational power of the IC, and indeed, systems-level studies have identified numerous important transformations in sound coding that occur in the IC. However, despite decades of effort, the cellular mechanisms underlying IC computations and how these computations change following hearing loss have remained largely impenetrable. In this review, we argue that this challenge persists due to the surprisingly difficult problem of identifying the neuron types and circuit motifs that comprise the IC. After summarizing the extensive evidence pointing to a diversity of neuron types in the IC, we highlight the successes of recent efforts to parse this complexity using molecular markers to define neuron types. We conclude by arguing that the discovery of molecularly identifiable neuron types ushers in a new era for IC research marked by molecularly targeted recordings and manipulations. We propose that the ability to reproducibly investigate IC circuits at the neuronal level will lead to rapid advances in understanding the fundamental mechanisms driving IC computations and how these mechanisms shift following hearing loss.
Topics: Humans; Inferior Colliculi; Auditory Pathways; Neurons; Brain Stem; Hearing Loss
PubMed: 38141518
DOI: 10.1016/j.heares.2023.108938 -
Brain Structure & Function Jul 2021Tinnitus is the perception of a 'ringing' sound without an acoustic source. It is generally accepted that tinnitus develops after peripheral hearing loss and is... (Review)
Review
Tinnitus is the perception of a 'ringing' sound without an acoustic source. It is generally accepted that tinnitus develops after peripheral hearing loss and is associated with altered auditory processing. The thalamus is a crucial relay in the underlying pathways that actively shapes processing of auditory signals before the respective information reaches the cerebral cortex. Here, we review animal and human evidence to define thalamic function in tinnitus. Overall increased spontaneous firing patterns and altered coherence between the thalamic medial geniculate body (MGB) and auditory cortices is observed in animal models of tinnitus. It is likely that the functional connectivity between the MGB and primary and secondary auditory cortices is reduced in humans. Conversely, there are indications for increased connectivity between the MGB and several areas in the cingulate cortex and posterior cerebellar regions, as well as variability in connectivity between the MGB and frontal areas regarding laterality and orientation in the inferior, medial and superior frontal gyrus. We suggest that these changes affect adaptive sensory gating of temporal and spectral sound features along the auditory pathway, reflecting dysfunction in an extensive thalamo-cortical network implicated in predictive temporal adaptation to the auditory environment. Modulation of temporal characteristics of input signals might hence factor into a thalamo-cortical dysrhythmia profile of tinnitus, but could ultimately also establish new directions for treatment options for persons with tinnitus.
Topics: Animals; Auditory Cortex; Auditory Pathways; Geniculate Bodies; Humans; Thalamus; Tinnitus
PubMed: 33934235
DOI: 10.1007/s00429-021-02284-x -
Journal of Neuroscience Research Jan 2024Tinnitus is a widespread public health issue that imposes a significant social burden. The occurrence and maintenance of tinnitus have been shown to be associated with... (Review)
Review
Tinnitus is a widespread public health issue that imposes a significant social burden. The occurrence and maintenance of tinnitus have been shown to be associated with abnormal neuronal activity in the auditory pathway. Based on this view, neurobiological and pharmacological developments in tinnitus focus on ion channels and synaptic neurotransmitter receptors in neurons in the auditory pathway. With major breakthroughs in the pathophysiology and research methodology of tinnitus in recent years, the role of the largest family of ion channels, potassium ion channels, in modulating the excitability of neurons involved in tinnitus has been increasingly demonstrated. More and more potassium channels involved in the neural mechanism of tinnitus have been discovered, and corresponding drugs have been developed. In this article, we review animal (mouse, rat, hamster, and guinea-pig), human, and genetic studies on the different potassium channels involved in tinnitus, analyze the limitations of current clinical research on potassium channels, and propose future prospects. The aim of this review is to promote the understanding of the role of potassium ion channels in tinnitus and to advance the development of drugs targeting potassium ion channels for tinnitus.
Topics: Cricetinae; Humans; Animals; Guinea Pigs; Mice; Rats; Potassium Channels; Tinnitus; Neurobiology; Auditory Pathways; Neurons
PubMed: 38284861
DOI: 10.1002/jnr.25281 -
Hearing Research Nov 2020Sensory input has profound effects on neuronal organization and sensory maps in the brain. The mechanisms regulating plasticity of the auditory pathway have been... (Review)
Review
Sensory input has profound effects on neuronal organization and sensory maps in the brain. The mechanisms regulating plasticity of the auditory pathway have been revealed by examining the consequences of altered auditory input during both developmental critical periods-when plasticity facilitates the optimization of neural circuits in concert with the external environment-and in adulthood-when hearing loss is linked to the generation of tinnitus. In this review, we summarize research identifying the molecular, cellular, and circuit-level mechanisms regulating neuronal organization and tonotopic map plasticity during developmental critical periods and in adulthood. These mechanisms are shared in both the juvenile and adult brain and along the length of the auditory pathway, where they serve to regulate disinhibitory networks, synaptic structure and function, as well as structural barriers to plasticity. Regulation of plasticity also involves both neuromodulatory circuits, which link plasticity with learning and attention, as well as ascending and descending auditory circuits, which link the auditory cortex and lower structures. Further work identifying the interplay of molecular and cellular mechanisms associating hearing loss-induced plasticity with tinnitus will continue to advance our understanding of this disorder and lead to new approaches to its treatment.
Topics: Auditory Cortex; Auditory Pathways; Deafness; Hearing Loss; Humans; Neuronal Plasticity; Tinnitus
PubMed: 32591097
DOI: 10.1016/j.heares.2020.107976