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 sensory hierarchy (e.g., auditory cortex). As such, virtually all proposed models to explain top-down facilitation are focused on the cerebral cortex, 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 stages of processing complements modulation at later (i.e., cortical) stages of processing. Finally, we suggest experimental approaches for future studies on this topic.

Corticofugal 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.…”

“…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 intracortical connections, with the massive system of descending cortico-fugal projections remaining unexplored (Asilador & Llano, 2020;Bastos et al, 2012).…”

Recurrent circuits amplify corticofugal signals and drive feedforward inhibition in the inferior colliculus

“…Feedback projections from the sensory neo-cortex to sub-cortical regions are ubiquitous in the mammalian brain. These corticofugal pathways enable “high-level”, cortical computations to rapidly control the nature of ascending sensory signals, thereby hypothetically supporting important “top-down” functions such as predictive coding, error propagation, or stream segregation (Briggs and Usrey, 2011; Stebbings et al, 2014; Usrey and Sherman, 2019; Asilador and Llano, 2020). Interestingly, corticofugal activity often has a net inhibitory effect upon spontaneous and sensory-evoked activity in sub-cortical circuits, consequently sharpening receptive fields and increasing the sparseness of neuronal representations along the ascending sensory hierarchy (Syka and Popelár, 1984; Zhang et al, 1997; Bledsoe et al, 2003; Boyd et al, 2012; Crandall et al, 2015; Vila et al, 2019; Born et al, 2021; but see Kirchgessner et al, 2021).…”

Patterns of Unilateral and Bilateral Projections From Layers 5 and 6 of the Auditory Cortex to the Inferior Colliculus in Mouse

“…Therefore, it is not surprising to find a bilateral projection system to the inferior colliculi, which also project to motor structures to mediate escape responses (Kawamura, 1975;Aitkin and Boyd, 1978;Edwards et al, 1979;Cadusseau and Roger, 1985;Appell and Behan, 1990;Huffman and Henson, 1990;Lesicko and Llano, 2020). The presence of a bilateral layer 6 system, which we have previously speculated to serve a modulatory role (Yudintsev et al, 2019;Asilador and Llano, 2020), was less expected, but may suggest that the dual functions of layer 5 and layer 6 are necessary for the potential escape function of the layer 5 corticofugal projections. The absence, then, of a bilateral projection to the LC may suggest that this region is less likely to be involved in rapid motor escape behaviors than DC.…”