Mixed representations of sound and action in the auditory midbrain

Quass, GL; Rogalla, MM; Ford, AN; Apostolides, PF

doi:10.1101/2023.09.19.558449

Cited by 8 publications

(4 citation statements)

References 111 publications

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“…Our recordings from corticorecipient neurons in the IC are consistent with previous studies demonstrating that neural representations of behavioral variables can be found in the auditory midbrain (Ruth et al, 1974;Nienhuis and Olds, 1978;Metzger et al, 2006;Gruters and Groh, 2012;Chen and Song, 2019;Yang et al, 2020;Saderi et al, 2021, Franceschi andBarkat, 2021;Shaheen et al, 2021;Quass et al, 2023). In keeping with responses recorded in the auditory cortex (Francis et al, 2018;Franceschi et al, 2021) and IC (Chen and Song 2019;Yang et al, 2020;Franceschi et al, 2021) of behaving mice, we found that the activity of most neurons was facilitated and about a third were suppressed during the sound detection task.…”

Section: Inferior Colliculus Neurons Exhibit Task-related Activitysupporting

confidence: 91%

Midbrain encodes sound detection behavior without auditory cortex

Lee

Weissenberger

King

et al. 2023

Preprint

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Hearing involves analyzing the physical attributes of sounds and integrating the results of this analysis with other sensory, cognitive and motor variables in order to guide adaptive behavior. The auditory cortex is considered crucial for the integration of acoustic and contextual information and is thought to share the resulting representations with subcortical auditory structures via its vast descending projections. By imaging cellular activity in the corticorecipient shell of the inferior colliculus of mice engaged in a sound detection task, we show that the majority of neurons encode information beyond the physical attributes of the stimulus and that the animals' behavior can be decoded from the activity of those neurons with a high degree of accuracy. Surprisingly, this was also the case in mice in which auditory cortical input to the midbrain had been removed by bilateral cortical lesions. This illustrates that subcortical auditory structures have access to a wealth of non-acoustic information and can, independently of the auditory cortex, carry much richer neural representations than previously thought.

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Section: Inferior Colliculus Neurons Exhibit Task-related Activitysupporting

confidence: 91%

Midbrain encodes sound detection behavior without auditory cortex

Lee

Weissenberger

King

et al. 2023

Preprint

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“…Non-auditory activity is also abundant in the IC of awake animals (Metzger et al, 2006;Yang et al, 2020;Shaheen et al, 2021;Quass et al, 2023), and seemingly persists in absence of corticofugal feedback (Lee et al, 2023). Thus it is currently unclear if non-auditory activity in corticofugal neurons is the cause, or rather the consequence of similar activity patterns in IC neurons.…”

Section: Dendritic Ca 2+ Spikes As Effectors Of Supervised Plasticitymentioning

confidence: 99%

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

Ford

Czarny

Rogalla

et al. 2022

Preprint

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Layer 5 pyramidal neurons of sensory cortices project corticofugal axons to myriad of sub-cortical targets, thereby broadcasting high-level signals important for perception and learning. Recent studies suggest dendritic Ca2+ spikes as key biophysical mechanisms supporting corticofugal neuron function: These long-lasting events drive burst firing, thereby initiating uniquely powerful signals to modulate sub-cortical representations and trigger learning-related plasticity. However, the behavioral relevance of corticofugal dendritic spikes is poorly understood. We shed light on this issue using 2-photon Ca2+ imaging of auditory corticofugal dendrites as mice engage in a sound-discrimination task. Unexpectedly, only a minority of dendritic spikes were triggered by sound. Rather, task-related dendritic activity mostly occurred following sound termination and reflected instrumental actions, irrespective of reward consumption. Temporally selective silencing of this motor-related activity impaired auditory discrimination learning. Thus, corticofugal systems contribution to learning and plasticity may be largely motor, rather than sensory in nature.

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“…Movement and expectation influence neural processing across many stages of the auditory pathway, from the ear to the cerebral cortex 11,33 . For example, sound-evoked responses are suppressed in the auditory thalamus during behavior 16 , movement-related signals are present in the inferior colliculus 34,35 , and self-generated sounds are suppressed as early as the dorsal cochlear nucleus (DCN) 13 . The presence of movement-related signals along the auditory neuroaxis has raised the question of where along this pathway prediction-related signals arise.…”

Section: Discussionmentioning

confidence: 99%

Learning within a sensory-motor circuit links action to expected outcome

Zhou,

Schneider

2024

Preprint

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The cortex integrates sound- and movement-related signals to predict the acoustic consequences of behavior and detect violations from expectations. Although expectation- and prediction-related activity has been observed in the auditory cortex of humans, monkeys, and mice during vocal and non-vocal acoustic behaviors, the specific cortical circuitry required for forming memories, recalling expectations, and making predictions remains unknown. By combining closed-loop behavior, electrophysiological recordings, longitudinal pharmacology, and targeted optogenetic circuit activation, we identify a cortical locus for the emergence of expectation and error signals. Movement-related expectation signals and sound-related error signals emerge in parallel in the auditory cortex and are concentrated in largely distinct neurons, consistent with a compartmentalization of different prediction-related computations. On a trial-by-trial basis, expectation and error signals are correlated in auditory cortex, consistent with a local circuit implementation of an internal model. Silencing the auditory cortex during motor-sensory learning prevents the emergence of expectation signals and error signals, revealing the auditory cortex as a necessary node for learning to make predictions. Prediction-like signals can be experimentally induced in the auditory cortex, even in the absence of behavioral experience, by pairing optogenetic motor cortical activation with sound playback, indicating that cortical circuits are sufficient for movement-like predictive processing. Finally, motor-sensory experience realigns the manifold dimensions in which auditory cortical populations encode movement and sound, consistent with predictive processing. These findings show that prediction-related signals reshape auditory cortex dynamics during behavior and reveal a cortical locus for the emergence of expectation and error.

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Mixed representations of sound and action in the auditory midbrain

Cited by 8 publications

References 111 publications

Midbrain encodes sound detection behavior without auditory cortex

Midbrain encodes sound detection behavior without auditory cortex

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

Learning within a sensory-motor circuit links action to expected outcome

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