Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections

Abstract

It has become widely accepted that humans use contextual information to infer the meaning of ambiguous acoustic signals. In speech, for example, high-level semantic, syntactic, or lexical information shape our understanding of a phoneme buried in noise. Most current theories to explain this phenomenon rely on hierarchical predictive coding models involving a set of Bayesian priors emanating from high-level brain regions (e.g., prefrontal cortex) that are used to influence processing at lower-levels of the cortical sensory hierarchy (e.g., auditory cortex). As such, virtually all proposed models to explain top-down facilitation are focused on intracortical connections, and consequently, subcortical nuclei have scarcely been discussed in this context. However, subcortical auditory nuclei receive massive, heterogeneous, and cascading descending projections at every level of the sensory hierarchy, and activation of these systems has been shown to improve speech recognition. It is not yet clear whether or how top-down modulation to resolve ambiguous sounds calls upon these corticofugal projections. Here, we review the literature on top-down modulation in the auditory system, primarily focused on humans and cortical imaging/recording methods, and attempt to relate these findings to a growing animal literature, which has primarily been focused on corticofugal projections. We argue that corticofugal pathways contain the requisite circuitry to implement predictive coding mechanisms to facilitate perception of complex sounds and that top-down modulation at early (i.e., subcortical) stages of processing complement modulation at later (i.e., cortical) stages of processing. Finally, we suggest experimental approaches for future studies on this topic.

Corticothalamic gating of population auditory thalamocortical transmission in mouse

“…Moreover, the strong association between the high probability of the OFF cortical responses and the low level of stimulation suggests that cortico-reticulothalamic control of thalamocortical transmission is most likely to be effective when signal-to-noise ratio is low. This finding is consistent with the notion that top-down modulation is mostly required for the attentional modulation of weak signals and that highly salient signals rely on bottom-up mechanisms to activate perceptual representations (reviewed in [45])Classical models have viewed sensory processing stations, including the thalamus and cortex, as a series of feedforward, hierarchically organized filters whereby combinations of receptive fields produce increasingly selective feature detectors, culminating in uniquely selective neurons [1,2]. This type of organization implies that moment-to-moment perception is a reflection of detailed streams of information coursing through ascending sensory systems, to be consciously perceived when those streams engage highly selective cells in the cortex.…”

Cortico-Fugal Regulation of Predictive Coding

“…Another possibility is that prediction errors are directly backpropagated from AC to IC. While this contradicts canonical predictive coding models, evidence for prediction error has been found in deep layers of the cortex in which feedback neurons reside (Asilador & Llano, 2020;Rummell et al, 2016). Though the precise mechanism underlying the generation of prediction error in IC remains unclear, our data show that feedback from AC plays a critical role in this process.…”

“…Virtually all models of hierarchical predictive coding to date have focused on intra-cortical connections, with the massive system of descending cortico-fugal projections remaining unexplored (Asilador & Llano, 2020;Bastos et al, 2012). Here, we investigated how inputs from AC to IC, the first station in the auditory system in which prediction error is found, shape metrics associated with predictive coding and deviance detection (Parras et al, 2017).…”

“…However, how feedback projections from AC shape predictive processing in subcortical targets has never been directly assessed. In fact, virtually all models of hierarchical predictive coding to date have focused on intra-cortical connections, with the massive system of descending cortico-fugal projections remaining unexplored (Asilador & Llano, 2020;Bastos et al, 2012).…”

Corticothalamic Pathways in Auditory Processing: Recent Advances and Insights From Other Sensory Systems

“…It is now widely accepted that the thalamus and CT pathways are engaged in high level computations previously thought to be exclusively cortical, such as language (Bartlett, 2013 ; Llano, 2013 ; Crosson, 2019 ; Mihai et al, 2019 ), learning and memory (Wolff and Vann, 2019 ), attention (Zhou et al, 2016 ; Schmitt et al, 2017 ), behavioral flexibility (Nakayama et al, 2018 ), and perceptual decision making (Halassa and Sherman, 2019 ). Recent evidence suggests that CT pathways may play a role in sensory attenuation of self-generated stimuli (Hua et al, 2020 ; Clayton et al, 2021 ) and perceptual inference (Bastos et al, 2012 ; Kanai et al, 2015 ; Auksztulewicz and Friston, 2016 ; Rikhye et al, 2018 ; Asilador and Llano, 2020 ).…”