Cell-type specific arousal-dependent modulation of thalamic activity in the lateral geniculate nucleus

Abstract

State dependent thalamocortical activity is important for sensory coding, oscillations and cognition. The lateral geniculate nucleus (LGN) relays visual information to the cortex, but the state dependent spontaneous and visually evoked activity of LGN neurons in awake behaving animals remains controversial. Using a combination of pupillometry, extracellular and intracellular recordings from identified LGN neurons we show that thalamocortical neurons and interneurons are distinctly correlated to arousal forming two complementary coalitions. Intracellular recordings indicated that the membrane potential of LGN TC neurons was tightly correlated to fluctuations in pupil size. Inactivating the corticothalamic feedback to the LGN suppressed the arousal dependency of LGN neurons. Taken together our results show that LGN neuronal membrane potential and action potential output are dynamically linked to arousal dependent brain states in awake mice and this might have important functional implications.

Pupil Size Dynamics Predict dLGN Firing Mode Over a Wide Range of Timescales

“…On the other hand, related work from our lab has shown that during locomotion the reduction in thalamic bursting and overall increase in firing rates still occurs even when CT feedback is optogenetically suppressed (Spacek et al, 2020). Together, these findings indicate that arousal-related modulations of thalamic activity involve both cortex-dependent and independent mechanisms (Molnár et al, 2021).…”

“…While raw pupil size has been successfully employed as a marker for internal arousal processes in sensory circuits (Augustinaite & Kuhn, 2020;Liang et al, 2020;Lin et al, 2019;McGinley et al, 2015a;Molnár et al, 2021;Petty et al, 2021;Schröder et al, 2020;Schwartz et al, 2020), other studies, including ours, have instead considered the pupil size signal as a continuous oscillatory process and focused on its dynamics (Reimer et al, 2014(Reimer et al, , 2016. We further extended this perspective by exploiting a decomposition method that respects the non-stationary, multi-scale nature of the pupil size signal (Huang et al, 1998), and found that several timescales were related to dLGN firing modes.…”

“…The results we have presented here, by separating spikes into tonic and burst, are limited to one fundamental characterization of activity patterns, and relate only to a single dimension of behavior. Other authors have observed a diversity in arousal-related modulations both between (Shimaoka et al, 2018;Williamson et al, 2015) and within (Aydın et al, 2018;Liang et al, 2020;Molnár et al, 2021;Schröder et al, 2020) sensory systems. Therefore future work will need to establish if other thalamic nuclei, or neuronal sub-types within the dLGN (Kerschensteiner & Guido, 2017;Piscopo et al, 2013;Rosón et al, 2019), are similarly modulated by pupil size dynamics.…”

Spiking activity in the visual thalamus is coupled to pupil dynamics across temporal scales

“…On the other hand, related work from our lab has shown that during locomotion the reduction in thalamic bursting and overall increase in firing rates still occurs even when CT feedback is optogenetically suppressed 83 . Together, these findings indicate that arousal-related modulations of thalamic activity involve both cortex-dependent and independent mechanisms 45 . Third, pupil-linked modulations have also been observed in retinal input to the dLGN 37 , which might be mediated by pre-synaptic modulation of the retinogeniculate synapse by serotonin 84 (5-HT).…”

“…While raw pupil size has been successfully employed as a marker for internal arousal processes in sensory circuits 10,15,18,22,37,39,[44][45][46] , other studies, including ours, have instead considered the pupil size signal as a continuous oscillatory process and focused on its dynamics 9,11,47 . We further extended this perspective by exploiting a decomposition method that respects the non-stationary, multi-scale nature of the pupil size signal 48 , and found that several timescales were related to dLGN firing modes.…”