Effects of arousal and movement on secondary somatosensory and visual thalamus

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.

Monosynaptic trans-collicular pathways link mouse whisker circuits to integrate somatosensory and motor cortical signals

“…Strikingly, we found that the whisker trigemino-collicular pathway sends abundant projections to the visual LP in the thalamus, providing an anatomical substrate for the recent findings that the LP integrates visual and tactile information (Petty et al, 2021). The integration of trans-collicular whisker signals in the LP may be an important mechanism underlying visuo-tactile functions such as hunting behavior, in which the SC has been shown to play a key role (Shang et al, 2019).…”

“…8). This result provides an anatomical substrate for the recent finding that the LP integrates visual and tactile information [45]. The integration of trans-collicular whisker signals in the LP may be an important mechanism underlying visuo-tactile functions such as hunting behavior, in which the SC has been shown to play a key role [7].…”

Visual thalamocortical mechanisms of waking state-dependent activity and alpha oscillations

“…Importantly, similar depolarizations also occurred during pupil dilations in the absence of overt movements of the whisker pad and the running wheel (Fig. S1), suggesting that a significant component of these signals may be associated with changes in arousal rather than movement per se (McGinley et al, 2015a;Petty et al, 2021), with the neural mechanisms of movement adding additional activating and information-containing (e.g. eye position, head direction) signals (Bouvier et al, 2020;Miura and Scanziani, 2021).…”

“…metabotropic vs. ionotropic receptors) and understanding these kinetics more fully would narrow the possible underlying mechanisms. Indeed, it is not yet fully known if the mechanisms of cortical activation that are associated with movement results from the activation of movement-related structures, or whether this brain activation represents arousal that is concomitant with movement (McGinley et al, 2015b;Petty et al 2021).…”

Transthalamic input to higher-order cortex selectively conveys state information

“…Consistent with a contextual role for LP, recent work found that LP thalamocortical axons projecting to higher visual cortex do not encode a detailed representation of optic flow, which is signaled by corticocortical axons, but rather discrepancies between optic flow and self-motion (Blot et al, 2021). Corticocortical afferents may thus be a principal conduit of feedforward sensory information between cortical areas, whereas higher-order thalamocortical axons may primarily contribute state-dependent contextual modulation of this sensory signaling (Petty et al, 2021; La Terra et al, 2022).…”