scholarly journals Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis

Author(s):  
Pia Brinkmann ◽  
Sonja A. Kotz ◽  
Jasper V. Smit ◽  
Marcus L. F. Janssen ◽  
Michael Schwartze

AbstractTinnitus 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.

2019 ◽  
Author(s):  
Paul Glad Mihai ◽  
Nadja Tschentscher ◽  
Katharina von Kriegstein

AbstractRecognising speech in background noise is a strenuous daily activity, yet most humans can master it. A mechanistic explanation of how the human brain deals with such sensory uncertainty is the Bayesian Brain Hypothesis. In this view, the brain uses a dynamic generative model to simulate the most likely trajectory of the speech signal. Such simulation account can explain why there is a task-dependent modulation of sensory pathway structures (i.e., the sensory thalami) for recognition tasks that require tracking of fast-varying stimulus properties (i.e., speech) in contrast to relatively constant stimulus properties (e.g., speaker identity) despite the same stimulus input. Here we test the specific hypothesis that this task-dependent modulation for speech recognition increases in parallel with the sensory uncertainty in the speech signal. In accordance with this hypothesis, we show—by using ultra-high-resolution functional magnetic resonance imaging in human participants—that the task-dependent modulation of the left primary sensory thalamus (ventral medial geniculate body, vMGB) for speech is particularly strong when recognizing speech in noisy listening conditions in contrast to situations where the speech signal is clear. Exploratory analyses showed that this finding was specific to the left vMGB; it was not present in the midbrain structure of the auditory pathway (left inferior colliculus, IC). The results imply that speech in noise recognition is supported by modifications at the level of the subcortical sensory pathway providing driving input to the auditory cortex.


2019 ◽  
Author(s):  
Paul Glad Mihai ◽  
Michelle Moerel ◽  
Federico de Martino ◽  
Robert Trampel ◽  
Stefan Kiebel ◽  
...  

AbstractSensory thalami are central sensory pathway stations for information processing. Their role for human cognition and perception, however, remains unclear. Recent evidence suggests a specific involvement of the sensory thalami in speech recognition. In particular, the auditory thalamus (medial geniculate body, MGB) response is modulated by speech recognition tasks and the amount of this task-dependent modulation is associated with speech recognition abilities. Here we tested the specific hypothesis that this behaviorally relevant modulation is present in the MGB subsection that corresponds to the primary auditory pathway (i.e., the ventral MGB [vMGB]). We used ultra-high field 7T fMRI to identify the vMGB, and found a significant positive correlation between the amount of task-dependent modulation and the speech recognition performance across participants within left vMGB, but not within the other MGB subsections. These results imply that modulation of thalamic driving input to the auditory cortex facilitates speech recognition.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Paul Glad Mihai ◽  
Michelle Moerel ◽  
Federico de Martino ◽  
Robert Trampel ◽  
Stefan Kiebel ◽  
...  

Sensory thalami are central sensory pathway stations for information processing. Their role for human cognition and perception, however, remains unclear. Recent evidence suggests an involvement of the sensory thalami in speech recognition. In particular, the auditory thalamus (medial geniculate body, MGB) response is modulated by speech recognition tasks and the amount of this task-dependent modulation is associated with speech recognition abilities. Here, we tested the specific hypothesis that this behaviorally relevant modulation is present in the MGB subsection that corresponds to the primary auditory pathway (i.e., the ventral MGB [vMGB]). We used ultra-high field 7T fMRI to identify the vMGB, and found a significant positive correlation between the amount of task-dependent modulation and the speech recognition performance across participants within left vMGB, but not within the other MGB subsections. These results imply that modulation of thalamic driving input to the auditory cortex facilitates speech recognition.


2002 ◽  
Vol 88 (3) ◽  
pp. 1433-1450 ◽  
Author(s):  
Michael P. Harms ◽  
Jennifer R. Melcher

Sound repetition rate plays an important role in stream segregation, temporal pattern recognition, and the perception of successive sounds as either distinct or fused. This study was aimed at elucidating the neural coding of repetition rate and its perceptual correlates. We investigated the representations of rate in the auditory pathway of human listeners using functional magnetic resonance imaging (fMRI), an indicator of population neural activity. Stimuli were trains of noise bursts presented at rates ranging from low (1–2/s; each burst is perceptually distinct) to high (35/s; individual bursts are not distinguishable). There was a systematic change in the form of fMRI response rate-dependencies from midbrain to thalamus to cortex. In the inferior colliculus, response amplitude increased with increasing rate while response waveshape remained unchanged and sustained. In the medial geniculate body, increasing rate produced an increase in amplitude and a moderate change in waveshape at higher rates (from sustained to one showing a moderate peak just after train onset). In auditory cortex (Heschl's gyrus and the superior temporal gyrus), amplitude changed somewhat with rate, but a far more striking change occurred in response waveshape—low rates elicited a sustained response, whereas high rates elicited an unusual phasic response that included prominent peaks just after train onset and offset. The shift in cortical response waveshape from sustained to phasic with increasing rate corresponds to a perceptual shift from individually resolved bursts to fused bursts forming a continuous (but modulated) percept. Thus at high rates, a train forms a single perceptual “event,” the onset and offset of which are delimited by the on and off peaks of phasic cortical responses. While auditory cortex showed a clear, qualitative correlation between perception and response waveshape, the medial geniculate body showed less correlation (since there was less change in waveshape with rate), and the inferior colliculus showed no correlation at all. Overall, our results suggest a population neural representation of the beginning and the end of distinct perceptual events that is weak or absent in the inferior colliculus, begins to emerge in the medial geniculate body, and is robust in auditory cortex.


Author(s):  
Ariel Gilad ◽  
Ido Maor ◽  
Adi Mizrahi

AbstractLearning to associate sensory stimuli with a chosen action has been classically attributed to the cortex. Whether the thalamus, considered mainly as an upstream area relative to cortex, encodes learning-related information is still largely unknown. We studied learning-related activity in the dorsal and medial regions of the medial geniculate body (MGB), part of the non-lemniscal auditory pathway. Using fiber photometry, we continuously imaged population calcium dynamics as mice learned a go/no-go auditory discrimination task. The MGB was tuned to frequency shortly after stimulus onset and responded to cognitive features like the choice of the mouse several hundred milliseconds later. Encoding of choice in the MGB increased with learning, and was highly correlated with the learning curves of the mice. MGB also encoded motor parameters of the mouse during the task. These results provide evidence that the MGB encodes task- motor- and learning-related information.


PLoS Biology ◽  
2021 ◽  
Vol 19 (6) ◽  
pp. e3001299
Author(s):  
Pilar Montes-Lourido ◽  
Manaswini Kar ◽  
Stephen V. David ◽  
Srivatsun Sadagopan

Early in auditory processing, neural responses faithfully reflect acoustic input. At higher stages of auditory processing, however, neurons become selective for particular call types, eventually leading to specialized regions of cortex that preferentially process calls at the highest auditory processing stages. We previously proposed that an intermediate step in how nonselective responses are transformed into call-selective responses is the detection of informative call features. But how neural selectivity for informative call features emerges from nonselective inputs, whether feature selectivity gradually emerges over the processing hierarchy, and how stimulus information is represented in nonselective and feature-selective populations remain open question. In this study, using unanesthetized guinea pigs (GPs), a highly vocal and social rodent, as an animal model, we characterized the neural representation of calls in 3 auditory processing stages—the thalamus (ventral medial geniculate body (vMGB)), and thalamorecipient (L4) and superficial layers (L2/3) of primary auditory cortex (A1). We found that neurons in vMGB and A1 L4 did not exhibit call-selective responses and responded throughout the call durations. However, A1 L2/3 neurons showed high call selectivity with about a third of neurons responding to only 1 or 2 call types. These A1 L2/3 neurons only responded to restricted portions of calls suggesting that they were highly selective for call features. Receptive fields of these A1 L2/3 neurons showed complex spectrotemporal structures that could underlie their high call feature selectivity. Information theoretic analysis revealed that in A1 L4, stimulus information was distributed over the population and was spread out over the call durations. In contrast, in A1 L2/3, individual neurons showed brief bursts of high stimulus-specific information and conveyed high levels of information per spike. These data demonstrate that a transformation in the neural representation of calls occurs between A1 L4 and A1 L2/3, leading to the emergence of a feature-based representation of calls in A1 L2/3. Our data thus suggest that observed cortical specializations for call processing emerge in A1 and set the stage for further mechanistic studies.


1978 ◽  
Vol 41 (2) ◽  
pp. 394-401 ◽  
Author(s):  
P. A. Hawrylyshyn ◽  
A. M. Rubin ◽  
R. R. Tasker ◽  
L. W. Organ ◽  
J. M. Fredrickson

1. Responses suggesting activation of the vestibular system, elicited by electrical stimulation of the human thalamus during 22 routine stereotaxic neurosurgical procedures, were examined in a retrospective study to determine the possible existence of vestibulothalamo-cortical projections in man. 2. Such responses were most frequently described as sensations of movement through space and were associated with two distinct vestibulothalamic projections: a) an anterior relay was situated ventral to the medial lemniscus, passing lateral to the red nucleus and dorsal to the subthalamic nucleus prior to terminating in the nucleus ventrointermedius (Vim) (comparable to VPLo in primates); b) a posterior relay associated with the auditory pathway (lateral lemniscus and brachium of the inferior colliculus) projected to the medial geniculate body. 3. The production of sensations of motion in conscious patients by stimulating areas that are similar to those reported constituting vestibulothalamic pathways in cats and primates implies a distinct primary sensory cortical projection for processing information from the vestibular receptors pertaining to the recognition of spatial movements.


2020 ◽  
Author(s):  
Aryo Zare ◽  
Gusta van Zwieten ◽  
Sonja A. Kotz ◽  
Yasin Temel ◽  
Benjamin G. Schultz ◽  
...  

AbstractBackgroundThe medial geniculate body (MGB) of the thalamus plays a central role in tinnitus pathophysiology. Breakdown of sensory gating in this part of the auditory thalamus is a potential mechanism underlying tinnitus. The alleviation of tinnitus-like behavior by high-frequency stimulation (HFS) of the MGB might mitigate dysfunctional sensory gating.ObjectiveThe study aims at exploring the role of the MGB in sensory gating as a mandatory relay area in auditory processing in noise-exposed and control subjects, and to assess the effect of MGB HFS on this function.MethodsNoise-exposed rats and controls were tested. Continuous auditory sequences were presented to allow assessment of sensory gating effects associated with pitch, binary grouping, and temporal regularity. Evoked potentials (EP) were recorded from the MGB and acquired before and after HFS (100 Hz).ResultsNoise-exposed rats showed differential modulation of MGB EP amplitudes, confirmed by significant main effects of stimulus type, pair position and temporal regularity. Noise-exposure selectively abolished the effect of temporal regularity on EP amplitudes. A significant three-way interaction between HFS phase, temporal regularity and rat condition (noise-exposed, control) revealed that only noise-exposed rats showed significantly reduced EP amplitudes following MGB HFS.ConclusionThis is the first report that shows thalamic filtering of incoming auditory signals based on different sound features. Noise-exposed rats further showed higher EP amplitudes in most conditions and did not differentiate the temporal regularity. Critically, MGB HFS was effective in reducing amplitudes of the EP responses in noise-exposed animals.HighlightsEP findings indicate sensory gating in the MGB in rats.Noise exposure alters EP amplitudes in the MGB.HFS selectively suppresses EP responses in noise-exposed animals.


2020 ◽  
Author(s):  
Gioia De Franceschi ◽  
Tania Rinaldi Barkat

Sensory processing varies depending on behavioral context. Here, we asked how task-engagement modulates neurons in the auditory system. We trained mice in a simple tone-detection task, and compared their neuronal activity during passive hearing and active listening. Electrophysiological extracellular recordings in the inferior colliculus, medial geniculate body, primary auditory cortex and anterior auditory field revealed widespread modulations across all regions and cortical layers, and in both putative regular and fast-spiking cortical neurons. Clustering analysis unveiled ten distinct modulation patterns that could either enhance or suppress neuronal activity. Task-engagement changed the tone-onset response in most neurons. Such modulations first emerged in subcortical areas, ruling out cortical feedback from primary auditory areas as the only mechanism underlying subcortical modulations. Half the neurons additionally displayed late modulations associated with licking, arousal or reward. Our results reveal the presence of functionally distinct subclasses of neurons, differentially sensitive to specific task-related variables but anatomically distributed along the auditory pathway.


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