Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex

Abstract

1 2 Recent research in mice indicates that luminance-independent fluctuations in pupil size predict 3 variability in spontaneous and evoked activity of single neurons in auditory and visual cortex. These 4 findings suggest that pupil is an indicator of large-scale changes in arousal state that affect sensory 5 processing. However, it is not known whether pupil-related state also influences the selectivity of 6 auditory neurons. We recorded pupil size and single-unit spiking activity in the primary auditory cortex 7 (A1) of non-anesthetized male and female ferrets during presentation of natural vocalizations and tone 8 stimuli that allow measurement of frequency and level tuning. Neurons showed a systematic increase in 9 both spontaneous and sound-evoked activity when pupil was large, as well as desynchronization and a 10 decrease in trial-to-trial variability. Relationships between pupil size and firing rate were non-11

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

“…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.…”

“…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. Finally, although the pupil size signal is often lauded as an index for internal modulations that occur in the absence of other overt behaviors, considering pupil size in the context of other behaviors such as locomotion (Reimer et al, 2014;Vinck et al, 2015) or eye movements (Schwartz et al, 2020) promises to reveal a more diverse coupling to neural measures. Indeed, expanding the notion of behavioral state to a high-dimensional set of latent behaviors has been successful in predicting neural activity, especially in thalamic neurons (Stringer et al, 2019).…”

“…Such spontaneous behaviors range from explicit motor actions, such as locomotion (Niell & Stryker, 2010), whisking (Crochet & Petersen, 2006), and orofacial movements (Stringer et al, 2019), to pupil size fluctuations that are thought to index changes in arousal (McGinley et al, 2015a;Reimer et al, 2014;Vinck et al, 2015). Indeed, although pupil size changes with ambient brightness, pupil dilation under constant illumination has been associated with hallmarks of arousal such as improved stimulus encoding (Lin et al, 2019;McGinley et al, 2015a;Reimer et al, 2014;Schwartz et al, 2020) as well as desynchronized low-amplitude, high-frequency cortical activity typical of active behavioral states (McGinley et al, 2015a;Lin et al, 2019;Reimer et al, 2014;Schwartz et al, 2020;Vinck et al, 2015). While pupil-linked arousal is often studied in cortical sensory areas, it is not yet clear what changes may be occurring at the level of the thalamic sensory nuclei that provide the cortex with sensory inputs.…”