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

Abstract

The corticothalamic (CT) pathways emanate from either Layer 5 (L5) or 6 (L6) of the neocortex and largely outnumber the ascending, thalamocortical pathways. The CT pathways provide the anatomical foundations for an intricate, bidirectional communication between thalamus and cortex. They act as dynamic circuits of information transfer with the ability to modulate or even drive the response properties of target neurons at each synaptic node of the circuit. L6 CT feedback pathways enable the cortex to shape the nature of its driving inputs, by directly modulating the sensory message arriving at the thalamus. L5 CT pathways can drive the postsynaptic neurons and initiate a transthalamic corticocortical circuit by which cortical areas communicate with each other. For this reason, L5 CT pathways place the thalamus at the heart of information transfer through the cortical hierarchy. Recent evidence goes even further to suggest that the thalamus via CT pathways regulates functional connectivity within and across cortical regions, and might be engaged in cognition, behavior, and perceptual inference. As descending pathways that enable reciprocal and context-dependent communication between thalamus and cortex, we venture that CT projections are particularly interesting in the context of hierarchical perceptual inference formulations such as those contemplated in predictive processing schemes, which so far heavily rely on cortical implementations. We discuss recent proposals suggesting that the thalamus, and particularly higher order thalamus via transthalamic pathways, could coordinate and contextualize hierarchical inference in cortical hierarchies. We will explore these ideas with a focus on the auditory system.

A Systematic Review of Direct Outputs from the Cerebellum to the Brainstem and Diencephalon in Mammals

“…In this classification, the reticular nucleus has a special status as it does not project to the cerebral cortex or the striatum, but instead provides inhibition to the other thalamic nuclei [344]. In turn, the cerebral cortex projects back to the thalamus, both directly as well as indirectly via the reticular nucleus, creating cortico-thalamo-cortical connections that facilitate information exchange between different cortical areas [344,[349][350][351][352].…”

Adaptation in auditory processing

“…Because nonlemniscal regions of the auditory midbrain and thalamus are heavily innervated by descending projections from the auditory cortex ( 251 , 252 ), we also have to consider whether stimulus-specific adaptation and deviance detection are controlled by the corticofugal system. A range of effects on subcortical repetition suppression and stimulus-specific adaptation has been reported following deactivation of the auditory cortex, the magnitude of which depends to some extent on the target structure and the methods used to manipulate the descending pathways ( 226 , 253 – 255 ).…”

Acute deletion of the central MR/GR steroid receptor correlates with changes in LTP, auditory neural gain, and GC-A cGMP signaling

“…It has been speculated that a critical input of auditory activity is necessary for the recruitment of a reinforcement process that interacts between the auditory thalamus, prefrontal cortex (PFC), and the hippocampus. Thus, the dorsal aspect of the MGB, which receives input from the primary auditory cortex and projects to higher-order auditory regions (Antunes and Malmierca, 2021;Mease and Gonzalez, 2021), is likely part of the topographically complex connectivity pattern projecting between the medio-dorsal thalamus, the medial PFC, and the hippocampal formation (Bueno-Junior and Leite, 2018). These corticofugal projections from the PFC influence auditory processing at lower levels of the cortical sensory hierarchy and often include activation of mesolimbic areas, such as the basolateral amygdala, the activation of which is involved in top-down feedback reinforcement processes (Asilador and Llano, 2020;Suga, 2020).…”

“…The medio-dorsal thalamus/PFC/hippocampal connectivity (see Figure 6) is not only sensitive to stress responses (for review, see Jett et al, 2017), but is also part of the extra-hypothalamic pathways involved in stress-control, emotional states, attention, and vigilance influenced by glucocorticoids (de Kloet et al, 2000(de Kloet et al, , 2019Wingenfeld and Otte, 2019;Antunes and Malmierca, 2021;Knipper et al, 2022). Interestingly, the TMX-induced deletion of MR in frontal brain regions resulted in enhanced ABR wave IV/I ratio (neural gain) and LTP.…”

“…Any adaptive central auditory responses following sound enrichment or acoustic trauma were found to be accompanied by increased hippocampal LTP levels (Matt et al, 2018;Likhtik and Johansen, 2019;Knipper et al, 2020;Marchetta et al, 2020b;Knipper et al, 2022;Manohar et al, 2022;Savitska et al, 2022;Zhang et al, 2022). The association between adaptive central auditory responses following sound enrichment or auditory trauma and LTP changes is suggested to be triggered through corticothalamic feedforward and feedback circuits (Antunes and Malmierca, 2021;Knipper et al, 2022). This encouraged us to investigate the influence of changed peripheral auditory processing in MR TMX cKO and GR TMX cKO (Marchetta et al, 2022) on central auditory responses of these animals in relation to short-and longterm hippocampal plasticity responses.…”