Corticothalamic Projections Deliver Enhanced-Responses to Medial Geniculate Body as a Function of the Temporal Reliability of the Stimulus

Kommajosyula, Srinivasa P.; Bartlett, Edward E.; Cai, Rui; Ling, Lynne; Caspary, Donald M.

doi:10.1101/2021.05.07.443156

Cited by 7 publications

(8 citation statements)

References 106 publications

(40 reference statements)

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“…Repetition enhancement has also been observed in the medial geniculate body in response to temporally degraded stimuli that are hypothesized to engage top-down resources to compensate for bottom-up acoustic information loss (Cai et al, 2016;Kommajosyula et al, 2019). Interestingly, this enhancement is reversed when cortico-thalamic pathways are blocked, further suggesting that repetition enhancement in the auditory system reflects a top-down phenomenon (Kommajosyula et al, 2021).…”

Section: Repetition Enhancement and Repetition Suppression In Icmentioning

confidence: 95%

Corticofugal regulation of predictive coding

Lesicko

Angeloni

Blackwell

et al. 2022

eLife

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Sensory systems must account for both contextual factors and prior experience to adaptively engage with the dynamic external environment. In the central auditory system, neurons modulate their responses to sounds based on statistical context. These response modulations can be understood through a hierarchical predictive coding lens: responses to repeated stimuli are progressively decreased, in a process known as repetition suppression, whereas unexpected stimuli produce a prediction error signal. Prediction error incrementally increases along the auditory hierarchy from the inferior colliculus (IC) to the auditory cortex (AC), suggesting that these regions may engage in hierarchical predictive coding. A potential substrate for top-down predictive cues is the massive set of descending projections from the auditory cortex to subcortical structures, although the role of this system in predictive processing has never been directly assessed. We tested the effect of optogenetic inactivation of the auditory cortico-collicular feedback in awake mice on responses of IC neurons to stimuli designed to test prediction error and repetition suppression. Inactivation of the cortico-collicular pathway led to a decrease in prediction error in IC. Repetition suppression was unaffected by cortico-collicular inactivation, suggesting that this metric may reflect fatigue of bottom-up sensory inputs rather than predictive processing. We also discovered populations of IC units that exhibit repetition enhancement, a sequential increase in firing with stimulus repetition. Cortico-collicular inactivation led to a decrease in repetition enhancement in the central nucleus of IC, suggesting that it is a top-down phenomenon. Negative prediction error, a stronger response to a tone in a predictable rather than unpredictable sequence, was suppressed in shell IC units during cortico-collicular inactivation. These changes in predictive coding metrics arose from bidirectional modulations in the response to the standard and deviant contexts, such that units in IC responded more similarly to each context in the absence of cortical input. We also investigated how these metrics compare between the anesthetized and awake states by recording from the same units under both conditions. We found that metrics of predictive coding and deviance detection differ depending on the anesthetic state of the animal, with negative prediction error emerging in the central IC and repetition enhancement and prediction error being more prevalent in the absence of anesthesia. Overall, our results demonstrate that the auditory cortex provides cues about the statistical context of sound to subcortical brain regions via direct feedback, regulating processing of both prediction and repetition.

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Section: Repetition Enhancement and Repetition Suppression In Icmentioning

confidence: 95%

Corticofugal regulation of predictive coding

Lesicko

Angeloni

Blackwell

et al. 2022

eLife

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“…However, repetition enhancement was observed in all three areas. Lesicko et al 2022 and Kommajosyula et al 2021 also found repetition enhancement in the IC and auditory thalamus of awake rodents, respectively. This is consistent with our findings that periodic target speaker sequences evoked stronger responses than random target speaker sequences (Fig.…”

Section: Discussionmentioning

confidence: 83%

Location-Specific Facilitation in Primate Auditory Cortex

Chen

Wang

et al. 2022

Preprint

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Responses of auditory cortex neurons are modulated by spectral or temporal context, but much less is known about modulation by spatial context. Here, we investigated single neuron responses to sequences of sounds either repeatedly delivered from a single spatial location or randomly delivered from multiple spatial locations in the auditory cortex of awake marmosets. Instead of inducing adaptation as expected from well-documented stimulus-specific adaptation studies, repetitive stimulation from a target speaker evoked long-lasting, location-specific facilitation (LSF) in many neurons, irrespective of the visibility of the target speaker. The extent of LSF decreased with decreasing presentation probability of the target speaker. Intracellular recordings showed that repetitive sound stimulation evoked sustained membrane potential depolarization which gave rise to firing rate facilitation. Computational models suggest two distinct neural mechanisms underlying LSF. Our findings revealed a novel form of contextual modulation in the auditory cortex that may play a role in auditory stream segregation.

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“…Furthermore, corticothalamic activation reduces adaptation to rapid repetitive stimulation as excitatory and inhibitory synaptic depression differs between the first-order visual/somatosensory thalamus and TRN (Mease et al, 2014;Crandall et al, 2015). In the auditory thalamus, corticothalamic activity seems to reduce adaptation to less-salient modulated noise since inactivation of corticothalamic neurons blocked the reduction (Kommajosyula et al, 2021). Therefore, corticothalamic neurons may be helpful for maintaining precise temporal responses in sequential or rapidly fluctuating sounds, which is characteristic of music and speech, and especially in less-salient sounds.…”

Section: Temporal Representation and Precisionmentioning

confidence: 99%

“…We postulate that corticothalamic feedback benefits other aspects of auditory scene analysis too. For example, enhanced signal detection by corticothalamic feedback seems to be robust for less salient inputs (Happel et al, 2014;Kommajosyula et al, 2021). Corticothalamic feedback may also contribute to signalin-noise processing by amplifying weak foreground sounds by controlling the gain of MGBv neurons.…”

Section: Selective Elimination Of Corticothalamic Neuronsmentioning

confidence: 99%

“…Along with musical training, corticothalamic feedback modulation may generally reinforce experience-dependent sound processing. Although speech processing ability degrades with aging, which is associated with impaired temporal coding and altered inhibitory signaling in the auditory system (Caspary et al, 2008;Gordon-Salant et al, 2011;Richardson et al, 2013;Presacco et al, 2016), temporal precision is actually improved in the MGB of aged-animals, which could indicate a compensation for the degraded hearing abilities via top-down modulation (Kommajosyula et al, 2019(Kommajosyula et al, , 2021Quraishe et al, 2020). Agedmusicians showed less degraded performance on the tasks that typically decline with aging (e.g., signal-in-noise, gap or mistuning detection) (Parbery-Clark et al, 2009;Zendel and Alain, 2012), which may reflect compensation via enhanced corticothalamic feedback.…”

Section: Clinical Relevancementioning

confidence: 99%

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Lemniscal Corticothalamic Feedback in Auditory Scene Analysis

Homma

Bajo

2021

Front. Neurosci.

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Sound information is transmitted from the ear to central auditory stations of the brain via several nuclei. In addition to these ascending pathways there exist descending projections that can influence the information processing at each of these nuclei. A major descending pathway in the auditory system is the feedback projection from layer VI of the primary auditory cortex (A1) to the ventral division of medial geniculate body (MGBv) in the thalamus. The corticothalamic axons have small glutamatergic terminals that can modulate thalamic processing and thalamocortical information transmission. Corticothalamic neurons also provide input to GABAergic neurons of the thalamic reticular nucleus (TRN) that receives collaterals from the ascending thalamic axons. The balance of corticothalamic and TRN inputs has been shown to refine frequency tuning, firing patterns, and gating of MGBv neurons. Therefore, the thalamus is not merely a relay stage in the chain of auditory nuclei but does participate in complex aspects of sound processing that include top-down modulations. In this review, we aim (i) to examine how lemniscal corticothalamic feedback modulates responses in MGBv neurons, and (ii) to explore how the feedback contributes to auditory scene analysis, particularly on frequency and harmonic perception. Finally, we will discuss potential implications of the role of corticothalamic feedback in music and speech perception, where precise spectral and temporal processing is essential.

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Corticothalamic Projections Deliver Enhanced-Responses to Medial Geniculate Body as a Function of the Temporal Reliability of the Stimulus

Cited by 7 publications

References 106 publications

Corticofugal regulation of predictive coding

Corticofugal regulation of predictive coding

Location-Specific Facilitation in Primate Auditory Cortex

Lemniscal Corticothalamic Feedback in Auditory Scene Analysis

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