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:10.1113/jp282321

Cited by 13 publications

(10 citation statements)

References 119 publications

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“…3J ), indicating that A1 feedback modulation may enhance the synchronized responses of MGB neurons to amplitude-modulated sounds. This is consistent with recently published work ( Kommajosyula et al. 2021 ).…”

Section: Resultssupporting

confidence: 94%

“…More specifically, we found corticothalamic modulations decreased spontaneous background activity and increased stimulus-driven response, resulting in increased SNR of MGB neurons during sensory processing. Moreover, A1 feedback modulation enhanced stimulus-synchronized responses of MGB neurons, consistent with recent awake research ( Kommajosyula et al. 2021 ).…”

Section: Discussionsupporting

confidence: 89%

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Selective corticofugal modulation on sound processing in auditory thalamus of awake marmosets

et al. 2022

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Cortical feedback has long been considered crucial for the modulation of sensory perception and recognition. However, previous studies have shown varying modulatory effects of the primary auditory cortex (A1) on the auditory response of subcortical neurons, which complicate interpretations regarding the function of A1 in sound perception and recognition. This has been further complicated by studies conducted under different brain states. In the current study, we used cryo-inactivation in A1 to examine the role of corticothalamic feedback on medial geniculate body (MGB) neurons in awake marmosets. The primary effects of A1 inactivation were a frequency-specific decrease in the auditory response of most MGB neurons coupled with an increased spontaneous firing rate, which together resulted in a decrease in the signal-to-noise ratio. In addition, we report for the first time that A1 robustly modulated the long-lasting sustained response of MGB neurons, which changed the frequency tuning after A1 inactivation, e.g. some neurons are sharper with corticofugal feedback and some get broader. Taken together, our results demonstrate that corticothalamic modulation in awake marmosets serves to enhance sensory processing in a manner similar to center-surround models proposed in visual and somatosensory systems, a finding which supports common principles of corticothalamic processing across sensory systems.

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Section: Resultssupporting

confidence: 94%

Section: Discussionsupporting

confidence: 89%

Selective corticofugal modulation on sound processing in auditory thalamus of awake marmosets

et al. 2022

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“…Repetition enhancement has also been observed in the MGB 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: Discussionmentioning

confidence: 99%

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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“…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 repetitive stimuli evoked facilitation, and periodic target speaker sequences evoked stronger responses than random target speaker sequences (Figure 5C).…”

Section: Discussionmentioning

confidence: 83%

“…Instead, our findings suggest that PE (i.e., repetition adaptation) and P (i.e., repetition facilitation) neurons coexist in the auditory cortex. The observation of auditory cortex inactivation reduces or blocks the repetition enhancement in the auditory midbrain and thalamus indicates prediction signals originate from P neurons in the auditory cortex (Lesicko et al, 2022; Kommajosyula et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

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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Corticothalamic projections deliver enhanced responses to medial geniculate body as a function of the temporal reliability of the stimulus

Cited by 13 publications

References 119 publications

Selective corticofugal modulation on sound processing in auditory thalamus of awake marmosets

Selective corticofugal modulation on sound processing in auditory thalamus of awake marmosets

Corticofugal regulation of predictive coding

Location-Specific Facilitation in Primate Auditory Cortex

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