Abstract
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.
Highlights
During active listening, sound features that are distracting, irrelevant, or totally predictable are often suppressed and do not rise to perceptual awareness (Atiani et al, 2009; Galindo-Leon et al, 2009; O’Connell et al, 2011; Lakatos et al, 2013; Shepard et al, 2016; Sohoglu and Chait, 2016; Southwell et al, 2017)
Their apical dendrites reside in superficial cortical layers, where they likely intermingle with inputs from frontal cortex that encode the cue or timing-related inputs initiated by the cue (Xu et al, 2012; Zhang et al, 2014; Takahashi et al, 2016).The axons of deep layer corticofugal neurons innervate subcortical central auditory targets including the medial geniculate body, inferior colliculus, superior olivary complex, and dorsal cochlear nucleus (Diamond et al, 1969; Suga and Ma, 2003; Winer, 2005; Stebbings et al, 2014)
We provide evidence that sensory and cognitive cues over multiple timescales enhance auditory perception, which provides a behavioral framework for future work that will monitor and manipulate corticofugal neurons during appropriate behaviors to identify their causal involvement in active listening
Summary
Sound features that are distracting, irrelevant, or totally predictable are often suppressed and do not rise to perceptual awareness (Atiani et al, 2009; Galindo-Leon et al, 2009; O’Connell et al, 2011; Lakatos et al, 2013; Shepard et al, 2016; Sohoglu and Chait, 2016; Southwell et al, 2017). The massive network of deep layer (L) auditory corticofugal projection neurons fulfill each of the requirements listed above and are a prime candidate for supporting temporally cued active listening Their apical dendrites reside in superficial cortical layers, where they likely intermingle with inputs from frontal cortex that encode the cue or timing-related inputs initiated by the cue (Xu et al, 2012; Zhang et al, 2014; Takahashi et al, 2016).The axons of deep layer corticofugal neurons innervate subcortical central auditory targets including the medial geniculate body, inferior colliculus, superior olivary complex, and dorsal cochlear nucleus (Diamond et al, 1969; Suga and Ma, 2003; Winer, 2005; Stebbings et al, 2014). As for the final requirement, a recent study from our lab discovered that layer L6 corticothalamic neurons, the largest component of the auditory corticofugal pathway, begin spiking hundreds of milliseconds prior to movements that trigger sounds and rewards (Clayton et al, 2021)
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