Effects of arousal and movement on secondary somatosensory and visual thalamus.

Amanda K Kinnischtzke,Gordon H Petty,Randy M Bruno,Y Kate Hong

doi:10.7554/elife.67611

Abstract

Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

Highlights

Somatosensory, visual, auditory, and gustatory cortex are each reciprocally connected with a specific subset of thalamic nuclei
To understand which components of whisking might drive posterior medial nucleus (POm) activity, we calculated the cross-correlation between POm firing rate and three features of whisking activity: the median angle across all whiskers (Figure 1D, gray), the amplitude metric which captures the slow envelope of whisking, and the median angle bandpass-filtered from 4-30 Hz, which reflects fast protractions and retractions of the whiskers
Our study tested the idea that secondary somatosensory thalamus is a monitor of movements or motor commands and manipulated the multiple known pathways to POm that could mediate such signals

Summary

Introduction

Somatosensory, visual, auditory, and gustatory cortex are each reciprocally connected with a specific subset of thalamic nuclei. These nuclei can be subdivided into primary and secondary (often termed “higher-order”) nuclei (Guillery and Sherman, 2002; Herkenham, 1980; Phillips et al, 2019). The primary nuclei are the main source of sensory input to the cortex and respond robustly to sensory stimulation with low latency (Chiaia et al, 1991; Constantinople and Bruno, 2013; Sherman and Guillery, 2002; Wimmer et al, 2010).

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