Cortical Stimulation Induces Excitatory Postsynaptic Potentials of Inferior Colliculus Neurons in a Frequency-Specific Manner

Qi, Jiyao; Zhang, Zizhen; He, Na; Liu, Xiuping; Zhang, Caseng; Yan, Jun

doi:10.3389/fncir.2020.591986

Cited by 11 publications

(8 citation statements)

References 69 publications

(100 reference statements)

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“…In the central auditory system, the corticofugal projection from auditory cortex to the inferior colliculus (IC) is of particular importance as the IC relays the majority of ascending acoustic signals destined for forebrain circuits. Accordingly, corticofugal activity powerfully shapes how IC neurons respond to diverse sound features, often via inhibitory interactions: Stimulating the auditory cortex dampens or completely suppresses IC acoustic responses (Syka and Popelár, 1984; Bledsoe et al, 2003; Vila et al, 2019; Blackwell et al, 2020), a result further corroborated by intracellular data showing that auditory cortex stimulation can drive synaptic inhibition in individual IC neurons (Mitani et al, 1983; Qi et al, 2020). Conversely, silencing auditory cortex often potentiates spontaneous and sound-evoked activity in the IC (Nwabueze-Ogbo et al, 2002; Popelár et al, 2003; Popelář et al, 2016; but see Zhang and Suga, 1997), indicating that ongoing auditory cortical activity can have a net inhibitory effect on the moment-to-moment excitability of IC neurons.…”

Section: Introductionmentioning

confidence: 87%

Recurrent circuits amplify corticofugal signals and drive feedforward inhibition in the inferior colliculus

Oberle¹,

Ford²,

Apostolides

2022

Preprint

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The inferior colliculus (IC) is a midbrain hub critical for perceiving complex, time-varying sounds such as speech. In addition to processing ascending inputs from most auditory brainstem nuclei, the IC receives descending inputs from auditory cortex that control IC neuron feature selectivity, plasticity, and certain forms of perceptual learning. Although these corticofugal synapses primarily release the excitatory transmitter glutamate, many physiology studies show that auditory cortical activity has a net inhibitory effect on IC neuron spiking. Perplexingly, anatomy studies indicate that corticofugal axons primarily target glutamatergic IC neurons while only sparsely innervating IC GABA neurons, thereby suggesting that corticofugal inhibition of the IC occurs largely independently of feedforward activation of local GABA neurons. We shed light on this paradox using in vitro electrophysiology and optogenetics in acute IC slices from fluorescent reporter mice. We find that corticofugal synaptic strength is indeed stronger onto IC glutamate compared to GABA neurons. Nevertheless, two mechanisms enable reliable corticofugal activation of local GABA neurons. 1) Many IC GABA neurons fire tonically at rest, such that sparse and weak excitation suffices to significantly increase their spike rates. 2) Corticofugal activity triggers barrages of large amplitude, polysynaptic EPSPs in IC GABA neurons, owing to a dense intra-collicular connectivity from local axon collaterals of IC glutamate neurons. Consequently, repetitive activity in corticofugal fibers drives spikes in IC GABA neurons and generates substantial recurrent inhibition. Thus, descending signals trigger intra-collicular inhibition despite apparent constraints of monosynaptic connectivity between auditory cortex and IC GABA neurons.

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Section: Introductionmentioning

confidence: 87%

Recurrent circuits amplify corticofugal signals and drive feedforward inhibition in the inferior colliculus

Oberle¹,

Ford²,

Apostolides

2022

Preprint

View full text Add to dashboard Cite

show abstract

“…The possible involvement of the auditory midbrain is consistent with reports that electrical or optogenetic stimulation of the of the inferior colliculus induces immediate motor responses [45,51], including vibrissae movement in anesthetized rats [53], while optogenetic activation of the auditory thalamus is not known to induce motor activity [18,54]. Inferior colliculus neurons can be suppressed by electrically or optogenetically activating auditory cortex [55,56] through recurrent inhibition in intracollicular circuits [57], though the net effect of cortical stimulation varies with activation parameters [55,58]. Conversely, silencing ACtx increases spontaneous and sound-evoked activity in the inferior colliculus [59].…”

Section: Discussionmentioning

confidence: 99%

Sound elicits stereotyped facial movements that provide a sensitive index of hearing abilities

Clayton,

Stecyk,

Guo

et al. 2023

Preprint

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SUMMARYSound elicits rapid movements of muscles in the face, ears, and eyes that protect the body from injury and trigger brain-wide internal state changes. Here, we performed quantitative facial videography from mice resting atop a piezoelectric force plate and observed that broadband sounds elicit rapid, small, and highly stereotyped movements of a facial region near the vibrissae array. Facial motion energy (FME) analysis revealed sensitivity to far lower sound levels than the acoustic startle reflex and greater reliability across trials and mice than sound-evoked pupil dilations or movement of other facial and body regions. FME tracked the low-frequency envelope of sounds and could even decode speech phonemes in varying levels of background noise with high accuracy. FME growth slopes were disproportionately steep in mice with autism risk gene mutations and noise-induced sensorineural hearing loss, providing an objective behavioral measure of sensory hyper-responsivity. Increased FME after noise-induced cochlear injury was closely associated with the emergence of excess gain in later waves of the auditory brainstem response, suggesting a midbrain contribution. Deep layer auditory cortex units were entrained to spontaneous facial movements but optogenetic suppression of cortical activity facilitated – not suppressed – sound-evoked FME, suggesting the auditory cortex is a modulator rather than a mediator of sound-evoked facial movements. These findings highlight a simple involuntary behavior that is more sensitive and integrative than other auditory reflex pathways and captures higher-order changes in sound processing from mice with inherited and acquired hearing disorders.

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“…While level and time differences are processed in brainstem nuclei, the inferior colliculus has been argued as being the first stage in which all three cues are combined (Slee and Young, 2011 ). Further, corticofugal modulation of sound processing or input selection of relevant stimuli or sound features is not only possible in the auditory thalamus (Guo et al, 2017 ) but has been shown throughout the auditory pathway (Malmierca et al, 2015 ; Suga, 2020 ; Asilador and Llano, 2021 ) including the cochlear nucleus (Luo et al, 2008 ) and the inferior colliculus (Nakamoto et al, 2008 ; Straka et al, 2015 ; Qi et al, 2020 ). Cooling of auditory cortex shifts the sensitivity of inferior colliculus neurons to interaural level cues (Nakamoto et al, 2008 ).…”

Section: Discussionmentioning

confidence: 99%

Effects of Cortical Cooling on Sound Processing in Auditory Cortex and Thalamus of Awake Marmosets

Jeschke

Ohl

Wang

2022

Front. Neural Circuits

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The auditory thalamus is the central nexus of bottom-up connections from the inferior colliculus and top-down connections from auditory cortical areas. While considerable efforts have been made to investigate feedforward processing of sounds in the auditory thalamus (medial geniculate body, MGB) of non-human primates, little is known about the role of corticofugal feedback in the MGB of awake non-human primates. Therefore, we developed a small, repositionable cooling probe to manipulate corticofugal feedback and studied neural responses in both auditory cortex and thalamus to sounds under conditions of normal and reduced cortical temperature. Cooling-induced increases in the width of extracellularly recorded spikes in auditory cortex were observed over the distance of several hundred micrometers away from the cooling probe. Cortical neurons displayed reduction in both spontaneous and stimulus driven firing rates with decreased cortical temperatures. In thalamus, cortical cooling led to increased spontaneous firing and either increased or decreased stimulus driven activity. Furthermore, response tuning to modulation frequencies of temporally modulated sounds and spatial tuning to sound source location could be altered (increased or decreased) by cortical cooling. Specifically, best modulation frequencies of individual MGB neurons could shift either toward higher or lower frequencies based on the vector strength or the firing rate. The tuning of MGB neurons for spatial location could both sharpen or widen. Elevation preference could shift toward higher or lower elevations and azimuth tuning could move toward ipsilateral or contralateral locations. Such bidirectional changes were observed in many parameters which suggests that the auditory thalamus acts as a filter that could be adjusted according to behaviorally driven signals from auditory cortex. Future work will have to delineate the circuit elements responsible for the observed effects.

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Cortical Stimulation Induces Excitatory Postsynaptic Potentials of Inferior Colliculus Neurons in a Frequency-Specific Manner

Cited by 11 publications

References 69 publications

Recurrent circuits amplify corticofugal signals and drive feedforward inhibition in the inferior colliculus

Recurrent circuits amplify corticofugal signals and drive feedforward inhibition in the inferior colliculus

Sound elicits stereotyped facial movements that provide a sensitive index of hearing abilities

Effects of Cortical Cooling on Sound Processing in Auditory Cortex and Thalamus of Awake Marmosets

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