Cortico-Fugal Regulation of Predictive Coding

Abstract

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. To assess the role of these projections in predictive coding, we optogenetically suppressed the auditory cortico-collicular feedback in awake mice while recording responses from IC neurons to stimuli designed to test prediction error and repetition suppression. Suppression 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 neurons that exhibit repetition enhancement, an increase in firing with stimulus repetition, and error suppression, a stronger response to a tone in a predictable rather than unpredictable context. Cortico-collicular suppression led to a decrease in repetition enhancement in the central nucleus and a reduction in error suppression in shell regions of IC. These changes in predictive coding metrics arose from bidirectional modulations in the response to the standard and deviant contexts, such that neurons in IC responded more similarly to each context in the absence of cortical input. 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.

Corticothalamic projections deliver enhanced responses to medial geniculate body as a function of the temporal reliability of the stimulus

“…2021; Lesicko et al . 2021). The current study was designed to examine the role of corticothalamic/top‐down projections to medial geniculate body (MGB) in mediating repetition adaptation/enhancement responses to repeating stimuli of different modulation depths.…”

“…Sensory adaptation has been observed in thalamus and cortex, for all sensory modalities, with declining responses for repeated stimuli (Ulanovsky et al 2003;Bartlett & Wang, 2005;Kohn, 2007;Maravall et al 2007;Pérez-González & Malmierca, 2014). In contrast to sensory adaptation, repetition enhancement to a repeating stimulus has been reported when acoustic signals were less temporally distinct, attended to, expected for statistical regularities, and/or with stimuli presented at higher rates in challenging conditions (Luce & Pisoni, 1998;Heinemann et al 2011;de Gardelle et al 2013;Müller et al 2013;Kommajosyula et al 2019;de Vries et al 2021;Lesicko et al 2021). The current study was designed to examine the role of corticothalamic/top-down projections to medial geniculate body (MGB) in mediating repetition adaptation/enhancement responses to repeating stimuli of different modulation depths.…”

Rule-based and stimulus-based cues bias auditory decisions via different computational and physiological mechanisms

“…These mechanisms affect neural responses throughout the auditory system and generally involve reduced responses to repeated presentation of the same stimuli and potentiated responses to novel (deviant) stimuli (10,26,27,64). There is debate over whether these phenomena reflect (top-down) predictions or whether they are indicative of traditionally construed bottom-up stimulus-specific adaptation, with evidence suggesting that both processes may contribute (2,(10)(11)(12)(13)(14)64,65). Both interpretations are consistent with our findings, in that the attractive effects could reflect predictions whereas the repulsive effects are more consistent with adaptation.…”

“…In contrast, stimulus-based expectations have been studied extensively and are thought to reflect, in part, bottom-up mechanisms in the auditory system including neural adaptation to stimulus regularities (3,(10)(11)(12)(13)(14). In general, these adaptation-like mechanisms can have the opposite effect as rule-based cues, including potentiating responses to violations of stimulus regularities and biasing perception away from recent stimuli (15)(16)(17)(18).…”