Task-induced modulations of neuronal activity along the auditory pathway

Franceschi, Gioia De; Barkat, Tania Rinaldi

doi:10.1101/2020.07.11.198481

Cited by 4 publications

(3 citation statements)

References 69 publications

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“…Sensory systems differentially encode environmental stimuli depending on the context in which they are encountered ( De Franceschi and Barkat, 2020 ; Herrmann et al, 2015 ; Jaramillo et al, 2014 ; Pakan et al, 2016 ; Takesian et al, 2018 ; Zhai et al, 2020 ). The same physical stimulus can elicit distinct neuronal responses depending on whether it is predictable or unexpected in a given sensory stream ( Weissbart et al, 2020 ; Yaron et al, 2012 ).…”

Section: Introductionmentioning

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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Section: Introductionmentioning

confidence: 99%

Corticofugal regulation of predictive coding

Lesicko

Angeloni

Blackwell

et al. 2022

eLife

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“…Finally, we used logistic regression to show that AAF activity during single trial could be predictive of the animal's performance (Figure 3). The neural activity during hit trials in the AAF could be influenced by the animal's general motivation (Fritz et al, 2003), motor related inputs (Schneider, 2020) or reward expectations (De Franceschi and Barkat, 2020).…”

Section: Discussionmentioning

confidence: 99%

Emergence and function of cortical offset responses in sound termination detection

Sołyga¹,

Barkat²

2021

Preprint

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Offset responses in auditory processing appear after a sound terminates. They arise in neuronal circuits within the peripheral auditory system, but their role in the central auditory system remains unknown. Here we ask what the behavioural relevance of cortical offset responses is and what circuit mechanisms drive them. At the perceptual level, our results reveal that experimentally minimizing auditory cortical offset responses decreases the mouse performance to detect sound termination, assigning a behavioural role to offset responses. By combining in vivo electrophysiology in the auditory cortex and thalamus of awake mice, we also demonstrate that cortical offset responses are not only inherited from the periphery but also amplified and generated de novo. Finally, we show that offset responses code more than silence, including relevant changes in sound trajectories. Together, our results reveal the importance of cortical offset responses in encoding sound termination and detecting changes within temporally discontinuous sounds crucial for speech and vocalization.

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“…First-order response modulation by arousal has been observed in multiple stages of the auditory pathway, even before auditory cortex. 51,52 Further, stochastic variability in the ascending auditory pathway may cause noise correlation in neurons that share ascending input. However, this seems unlikely as this type of noise has been reported to be very weak in cortex.…”

Section: Separate Circuitry Drives First-and Second-order Neural Varimentioning

confidence: 99%

Selective effects of arousal on population coding of natural sounds in auditory cortex

Heller

Schwartz

Saderi

et al. 2020

Preprint

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In addition to encoding sound stimulus features, activity in primary auditory cortex (A1) is modulated by non-sensory behavioral state variables, including arousal. Here, we investigated how arousal, measured by pupil size, influences stimulus discriminability in A1. To do this, we recorded from populations of A1 neurons in awake animals while presenting a diverse set of natural sound stimuli. In contrast to previous work, the large stimulus set allowed us to investigate effects of arousal across a wide range of sensory response space. Arousal consistently increased evoked response magnitude and reduced pairwise noise correlations. On average, these changes improved the accuracy of the neural code. However, effects varied across stimuli; neural coding was most improved for areas of the sensory space where noise correlations interfered with the sensory discrimination axis. We also found that first-order modulation of evoked responses and second-order modulation of correlated variability acted on distinct neural populations and timescales, suggesting that arousal interacts with multiple circuits underlying activity in A1.

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Task-induced modulations of neuronal activity along the auditory pathway

Cited by 4 publications

References 69 publications

Corticofugal regulation of predictive coding

Corticofugal regulation of predictive coding

Emergence and function of cortical offset responses in sound termination detection

Selective effects of arousal on population coding of natural sounds in auditory cortex

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