Stimulus-specific prediction error neurons in mouse auditory cortex

Audette, Nicholas J.; Schneider, David M.

doi:10.1101/2023.01.06.523032

Cited by 10 publications

(11 citation statements)

References 41 publications

(59 reference statements)

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“…Expectation-like signals are also present in our analyses of population dynamics, where we observe an alignment of sound-encoding and movement-encoding dimensions following extensive experience with a sound-generating movement. Predictive processing during behavior has been extensively studied in sensory cortex (Schneider et al, 2018; Audette et al, 2022; Audette et al, 2023; Keller et al, 2012) and our data suggest that motor cortex may also be involved in forming expectations and encoding violations.…”

Section: Discussionmentioning

confidence: 64%

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Sensation and expectation are embedded in mouse motor cortical activity

Holey,

Schneider

2023

Preprint

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During behavior, the motor cortex sends copies of motor-related signals to sensory cortices. It remains unclear whether these corollary discharge signals strictly encode movement or whether they also encode sensory experience and expectation. Here, we combine closed-loop behavior with large-scale physiology, projection-pattern specific recordings, and circuit perturbations to show that neurons in mouse secondary motor cortex (M2) encode sensation and are influenced by expectation. When a movement unexpectedly produces a sound, M2 becomes dominated by sound-evoked activity. Sound responses in M2 are inherited partially from the auditory cortex and are routed back to the auditory cortex, providing a path for the dynamic exchange of sensory-motor information during behavior. When the acoustic consequences of a movement become predictable, M2 responses to self-generated sounds are selectively gated off. These changes in single-cell responses are reflected in population dynamics, which are influenced by both sensation and expectation. Together, these findings reveal the rich embedding of sensory and expectation signals in motor cortical activity.

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Section: Discussionmentioning

confidence: 64%

“…from M2). In the auditory cortex, experience with a sound-generating behavior results in the selective suppression of a movement’s expected consequences but weaker or no suppression when the same movement makes an unexpected sound (Schneider et al, 2018; Rummel et al, 2016; Audette et al, 2022; Audette et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Sensation and expectation are embedded in mouse motor cortical activity

Holey,

Schneider

2023

Preprint

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“…Within the auditory cortex, two prediction-like signals are consistent with the local implementation of an internal model. First, auditory cortical responses to expected self-generated sounds tend to be weak, whereas the same neurons’ responses to unexpected sounds tend to be large, consistent with the auditory cortex signaling a prediction error 17–19 . Second, during a sound-generating behavior, movement-related signals in the auditory cortex become concentrated in neurons tuned to the expected sound and this activity peaks at the time the sound is expected to occur (even if the sound is omitted) 16,17 .…”

Section: Introductionmentioning

confidence: 64%

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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“…Finally, we investigated the representational format of prediction errors (PEs) in the unexpected conditions. We operate under the premise that PEs in high-level cortex do not merely signaling surprise, but are teaching signals 19 carrying feature-specific content 7, 20, 21 . Our results so far suggest that lower areas inherit tuning properties from higher areas through predictions.…”

Section: Resultsmentioning

confidence: 99%

Predictions enable top-down pattern separation in the macaque face-processing hierarchy

Nigam,

Schwiedrzik

2023

Preprint

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SummaryDistinguishing faces requires well distinguishable neural activity patterns. Contextual information may separate neural representations, leading to enhanced identity recognition. Here, we investigate how predictions derived from contextual information affect the separability of neural activity patterns in the macaque face-processing system, a 3-level processing hierarchy in ventral visual cortex. We find that in the presence of predictions, early stages of this hierarchy exhibit well separable and high-dimensional neural geometries otherwise characteristic only of the top of the hierarchy. This is accompanied by a systematic shift of tuning properties from higher to lower areas, endowing lower areas with higher-order, invariant representations instead of their feedforward tuning properties. Thus, top-down signals dynamically transform neural representations of faces into separable and high-dimensional neural geometries. Our results provide evidence how predictive context transforms flexible representational spaces to optimally use the computational resources provided by cortical processing hierarchies for better and faster distinction of facial identities.HighlightsPredictions increase pattern-separation and dimensionality in early face-processing areas.Early face-processing areas dynamically inherit tuning properties from higher areas.Predictions enable top-down separability and invariance for identity recognition.

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Stimulus-specific prediction error neurons in mouse auditory cortex

Cited by 10 publications

References 41 publications

Sensation and expectation are embedded in mouse motor cortical activity

Sensation and expectation are embedded in mouse motor cortical activity

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

Predictions enable top-down pattern separation in the macaque face-processing hierarchy

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