Abstract
Pupil diameter is often treated as a noninvasive readout of activity in the locus coeruleus (LC). However, how accurately it can be used to index LC activity is not known. To address this question, we established a graded relationship between pupil size changes and LC spiking activity in mice, where pupil dilation increased monotonically with the number of LC spikes. However, this relationship exists with substantial variability such that pupil diameter can only be used to accurately predict a small fraction of LC activity on a moment-by-moment basis. In addition, pupil exhibited large session-to-session fluctuations in response to identical optical stimulation in the LC. The variations in the pupil-LC relationship were strongly correlated with decision bias-related behavioral variables. Together, our data show that substantial variability exists in an overall graded relationship between pupil diameter and LC activity, and further suggest that the pupil-LC relationship is dynamically modulated by brain states, supporting and extending our previous findings (Yang et al., 2021).
Highlights
Fluctuations of brain states, such as arousal and attention, strongly impact sensory processing, decision-making, and animal behavior (Harris and Thiele, 2011; Lee and Dan, 2012; Thiele and Bellgrove, 2018; Petersen, 2019; McCormick et al, 2020)
We established a graded relationship between pupil and locus coeruleus (LC), where pupil dilation increased monotonically with LC spiking activity. This relationship exists with substantial variability such that pupil size changes can only accurately predict a small fraction of LC spiking on a moment-b y-m oment basis
Using optogenetics to activate LC neurons, we showed that pupil responses exhibited large session-to-session fluctuations to identical optical stimulation, despite stable LC responses
Summary
Fluctuations of brain states, such as arousal and attention, strongly impact sensory processing, decision-making, and animal behavior (Harris and Thiele, 2011; Lee and Dan, 2012; Thiele and Bellgrove, 2018; Petersen, 2019; McCormick et al, 2020). We do not know whether and how pupil diameter can be used to make accurate inferences of LC activity on a moment-by-moment basis To address these questions, we recorded spiking activity from optogenetically tagged LC neurons simultaneously with pupil diameter in head-fixed mice trained to perform a tactile detection task (McBurney-Lin et al, 2020; Yang et al, 2021). We established a graded relationship between pupil and LC, where pupil dilation increased monotonically with LC spiking activity This relationship exists with substantial variability such that pupil size changes can only accurately predict a small fraction of LC spiking on a moment-b y-m oment basis. Our work further suggests that brain states dynamically modulate the coupling between pupil and LC
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