Auditory corticofugal neurons transmit auditory and non-auditory information during behavior

Ford, Alexander N; Czarny, Jordyn; Rogalla, Meike M; Quass, Gunnar L; Apostolides, Pierre F.

doi:10.1101/2022.08.08.503214

Cited by 5 publications

(5 citation statements)

References 127 publications

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“…In L2/3 and L4, only 11% of RS units exhibited significant spike rate modulation during spontaneous facial movements (all positively modulated), whereas 26% of units in L5 and L6 were significantly modulated (17% positively modulated), (Figure 6C-D). A more granular analysis of spike rate modulation by depth confirmed prior reports that deep layer auditory cortex (ACtx) neurons are more strongly recruited by movement (Figure 6E) [32][33][34][35].…”

Section: Suppressing Auditory Cortex Neural Activity Enhances Sound-e...supporting

confidence: 81%

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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Section: Suppressing Auditory Cortex Neural Activity Enhances Sound-e...supporting

confidence: 81%

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

Clayton,

Stecyk,

Guo

et al. 2023

Preprint

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“…One potential candidate is the massive system of descending auditory cortical projections. Indeed, auditory cortico-collicular neurons preferentially target the non-lemniscal shell IC layers (Bajo et al, 2007; Winer, 2005; Yudintsev et al, 2021), and are highly active during the response period in a similar instrumental task to the one employed here (Ford et al, 2022). However, auditory cortex lesions apparently reduce, but do not abolish putative non-auditory activity in cortico-recipient IC neurons (Lee et al, 2023), suggesting that shell IC neurons could inherit task-relevant activity from non-cortical sources.…”

Section: Discussionmentioning

confidence: 89%

Mixed representations of sound and action in the auditory midbrain

Quass,

Rogalla,

Ford

et al. 2023

Preprint

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Linking sensory input and its consequences is a fundamental brain operation. Accordingly, neural activity of neo-cortical and limbic systems often reflects dynamic combinations of sensory and behaviorally relevant variables, and these mixed representations are suggested to be important for perception, learning, and plasticity. However, the extent to which such integrative computations might occur in brain regions upstream of the forebrain is less clear. Here, we conduct cellular-resolution 2-photon Ca2+ imaging in the superficial shell layers of the inferior colliculus (IC), as head-fixed mice of either sex perform a reward-based psychometric auditory task. We find that the activity of individual shell IC neurons jointly reflects auditory cues and actions, such that trajectories of neural population activity diverge depending on behavioral choice. Consequently, simple classifier models trained on shell IC neuron activity can predict trial-by-trial outcomes, even when training data are restricted to neural activity occurring prior to instrumental actions. Thus in behaving animals, auditory midbrain neurons transmit a population code that reflects a joint representation of sound and action.

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“…Thus, observing topographical CC activity patterns in a behavioral (possibly learning-related) context might be the only way to definitively describe their role in providing frequency-specific feedback to the IC. Ford et al (2022) imaged activity in dendrites of CC neurons during behavior and concluded that they contribute to learning by transmitting non-auditory signals. However, they did not report on topographical aspects.…”

Section: Discussionmentioning

confidence: 99%

Distinct topographic organization and network activity patterns of corticocollicular neurons within layer 5 auditory cortex

Schmitt,

Andrea,

Wadle

et al. 2023

Front. Neural Circuits

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The auditory cortex (AC) modulates the activity of upstream pathways in the auditory brainstem via descending (corticofugal) projections. This feedback system plays an important role in the plasticity of the auditory system by shaping response properties of neurons in many subcortical nuclei. The majority of layer (L) 5 corticofugal neurons project to the inferior colliculus (IC). This corticocollicular (CC) pathway is involved in processing of complex sounds, auditory-related learning, and defense behavior. Partly due to their location in deep cortical layers, CC neuron population activity patterns within neuronal AC ensembles remain poorly understood. We employed two-photon imaging to record the activity of hundreds of L5 neurons in anesthetized as well as awake animals. CC neurons are broader tuned than other L5 pyramidal neurons and display weaker topographic order in core AC subfields. Network activity analyses revealed stronger clusters of CC neurons compared to non-CC neurons, which respond more reliable and integrate information over larger distances. However, results obtained from secondary auditory cortex (A2) differed considerably. Here CC neurons displayed similar or higher topography, depending on the subset of neurons analyzed. Furthermore, specifically in A2, CC activity clusters formed in response to complex sounds were spatially more restricted compared to other L5 neurons. Our findings indicate distinct network mechanism of CC neurons in analyzing sound properties with pronounced subfield differences, demonstrating that the topography of sound-evoked responses within AC is neuron-type dependent.

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Auditory corticofugal neurons transmit auditory and non-auditory information during behavior

Cited by 5 publications

References 127 publications

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

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

Mixed representations of sound and action in the auditory midbrain

Distinct topographic organization and network activity patterns of corticocollicular neurons within layer 5 auditory cortex

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