The engagement of layer 6 corticothalamic neurons in somatosensation.

Abstract

The corticothalamic neurons from layer 6 (L6CT) of primary sensory cortices provide extensive input to the thalamus in addition to projecting across layers intracortically, positioning them to play a key hypothesized role in shaping thalamocortical signaling. With the expansion of tools for precise functional identification of L6CT neurons during in-vivo electrophysiology, increasing evidence highlights L6CT neurons as dynamic gain modulators of thalamocortical sensory responses. However, much of the work to date has been conducted under anesthesia and not in the context of awake and/or behaving animals. In this study, we show in the awake mouse that L6CT neurons convey information about the ascending sensory input, the timing of which is fast enough to contribute to the sensory response of neurons throughout the thalamocortical circuit. Overall, L6CT neurons robustly encode the presence vs absence of a sensory stimulus but are relatively weak encoders of the fine details. Benchmarked against the activity of other excitatory cortical neurons, we also provide evidence for L6CT neurons as predictors of behavioral outcome during a trained detection task. Taken together, the results in this study potentially tie L6CT neurons to behavior in tactile detection, one of the most fundamental functional roles of the pathway.

Significance statement: Layer 6 corticothalamic (L6CT) neurons provide one of the major feedback pathways from the sensory cortex to the thalamus, yet the extent to which their role in sensory processing remains poorly understood. We show that L6CT neurons in mouse somatosensory cortex robustly signal the presence of tactile stimuli but are comparatively weak encoders of stimulus strength. During a sensory detection task, their responses strongly reflect whether the animal detects the stimulus and predict behavioral outcome better than other cortical excitatory neurons. These findings suggest that L6CT neurons are specialized less for representing fine sensory detail and more for signaling the occurrence and behavioral relevance of sensory events, providing insight into when and how corticothalamic feedback participates in perception.