Inverted central auditory hierarchies for encoding local intervals and global temporal patterns

Asokan, Meenakshi M.; Williamson, R. S.; Hancock, Kenneth E.; Polley, Daniel B.

doi:10.1016/j.cub.2021.01.076

Cited by 27 publications

(22 citation statements)

References 57 publications

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“…Using 9.4 T fMRI in marmosets, we found the neural responses to the local novelty in the IC, MG and primary auditory cortex. Our finding is consistent with a recent mice study with electrophysiological recordings in these regions, where the authors examined local intervals (0.001 -0.1 s) separating consecutive noise bursts and global rhythmic patterns (~ 1 s) of inter-burst interval sequences (Asokan et al, 2021). They showed that neural response to local intervals was strong in the IC, but declined across MG and primary auditory cortex; the response to global rhythmic patterns was robust in primary auditory, but weak in MG and IC.…”

Section: Predictive Signals In the Subcortical Areas Along Auditory Pathwaysupporting

confidence: 93%

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Jiang

Komatsu

Chen

et al. 2021

Preprint

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Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hierarchical depth and its neural mechanisms, remains largely unexplored. Here, we investigated the hierarchical depth of predictive auditory processing by combining functional magnetic resonance imaging (fMRI) and high-density whole-brain electrocorticography (ECoG) in marmoset monkeys during an auditory local-global paradigm in which the temporal regularities of the stimuli were designed at two hierarchical levels. The prediction-errors and prediction updates were examined as neural responses to auditory mismatches and omissions. Using fMRI, we identified a hierarchical gradient along the auditory pathway: midbrain and sensory regions represented local, short-time-scale predictive processing followed by associative auditory regions, whereas anterior temporal and prefrontal areas represented global, long-time-scale sequence processing. The complementary ECoG recordings confirmed the activations at cortical surface areas and further differentiated the signals of prediction-error and update, which were transmitted via putatively bottom-up γ and top-down β oscillations, respectively. Furthermore, omission responses caused by absence of input, reflecting solely the two levels of prediction signals that are unique to the hierarchical predictive coding framework, demonstrated the hierarchical predictions in the auditory, temporal, and prefrontal areas. Thus, our findings support the hierarchical predictive coding framework, and outline how neural circuits and spatiotemporal dynamics are used to represent and arrange a hierarchical structure of auditory sequences in the marmoset brain.

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Section: Predictive Signals In the Subcortical Areas Along Auditory Pathwaysupporting

confidence: 93%

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Jiang

Komatsu

Chen

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…Furthermore, the prediction-error responses have been widely investigated in the subcortical auditory areas of humans (Escera & Malmierca, 2014) and animals (Parras et al, 2017), which support a large-scale hierarchical organization of auditory processing. Our finding is also consistent with a recent mouse study with electrophysiological recordings in these regions, where the authors examined local intervals (0.001 -0.1 s) separating consecutive noise bursts and global rhythmic patterns (~ 1 s) of inter-burst interval sequences (Asokan et al, 2021). They showed that neural responses to local intervals were strong in the IC, but attenuated across MG and primary auditory cortex; the response to global rhythmic patterns was robust in primary auditory, but weak in MG and IC.…”

Section: Predictive Signals In the Subcortical Areas Along Auditory P...supporting

confidence: 92%

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Jiang

Komatsu

Chen

et al. 2022

eLife

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Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hierarchical depth and its neural mechanisms, remains largely unexplored. Here, we investigated the hierarchical depth of predictive auditory processing by combining functional magnetic resonance imaging (fMRI) and high-density whole-brain electrocorticography (ECoG) in marmoset monkeys during an auditory local-global paradigm in which the temporal regularities of the stimuli were designed at two hierarchical levels. The prediction-errors and prediction updates were examined as neural responses to auditory mismatches and omissions. Using fMRI, we identified a hierarchical gradient along the auditory pathway: midbrain and sensory regions represented local, shorter-time-scale predictive processing followed by associative auditory regions, whereas anterior temporal and prefrontal areas represented global, longer-time-scale sequence processing. The complementary ECoG recordings confirmed the activations at cortical surface areas and further differentiated the signals of prediction-error and update, which were transmitted via putative bottom-up g and top-down b oscillations, respectively. Furthermore, omission responses caused by absence of input, reflecting solely the two levels of prediction signals that are unique to the hierarchical predictive coding framework, demonstrated the hierarchical top-down process of predictions in the auditory, temporal, and prefrontal areas. Thus, our findings support the hierarchical predictive coding framework, and outline how neural networks and spatiotemporal dynamics are used to represent and arrange a hierarchical structure of auditory sequences in the marmoset brain.

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“…Our behavioral data show that top-down influences related to temporal expectations enhance even basic perceptual abilities like tone detection or recognition. Changes in basic auditory processing driven by top-down influences suggest a scheme where long-range inputs from brain areas involved in generating temporal expectations would modulate the fasttimescale, fine-grained encoding of acoustic features, which is generally restricted to the beginning of the central auditory pathway (Joris et al, 2004;Asokan et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Behavioral Approaches to Study Top-Down Influences on Active Listening

et al. 2021

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The massive network of descending corticofugal projections has been long-recognized by anatomists, but their functional contributions to sound processing and auditory-guided behaviors remain a mystery. Most efforts to characterize the auditory corticofugal system have been inductive; wherein function is inferred from a few studies employing a wide range of methods to manipulate varying limbs of the descending system in a variety of species and preparations. An alternative approach, which we focus on here, is to first establish auditory-guided behaviors that reflect the contribution of top-down influences on auditory perception. To this end, we postulate that auditory corticofugal systems may contribute to active listening behaviors in which the timing of bottom-up sound cues can be predicted from top-down signals arising from cross-modal cues, temporal integration, or self-initiated movements. Here, we describe a behavioral framework for investigating how auditory perceptual performance is enhanced when subjects can anticipate the timing of upcoming target sounds. Our first paradigm, studied both in human subjects and mice, reports species-specific differences in visually cued expectation of sound onset in a signal-in-noise detection task. A second paradigm performed in mice reveals the benefits of temporal regularity as a perceptual grouping cue when detecting repeating target tones in complex background noise. A final behavioral approach demonstrates significant improvements in frequency discrimination threshold and perceptual sensitivity when auditory targets are presented at a predictable temporal interval following motor self-initiation of the trial. Collectively, these three behavioral approaches identify paradigms to study top-down influences on sound perception that are amenable to head-fixed preparations in genetically tractable animals, where it is possible to monitor and manipulate particular nodes of the descending auditory pathway with unparalleled precision.

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Inverted central auditory hierarchies for encoding local intervals and global temporal patterns

Cited by 27 publications

References 57 publications

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Behavioral Approaches to Study Top-Down Influences on Active Listening

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