Abstract
Several physiology signals, including heart rate and pupil size, have been widely used as peripheral indices of arousal to evaluate the effects of arousal on brain functions. However, whether behavior depends differently on arousal indexed by these physiological signals remains unclear. We simultaneously recorded electrocardiogram (ECG) and pupil size in head-fixed rats performing tactile discrimination tasks. We found both heartbeat dynamics and pupil size co-varied with behavioral outcomes, indicating behavior was dependent upon arousal indexed by the two physiological signals. To estimate the potential difference between the effects of pupil-linked arousal and heart rate-linked arousal on behavior, we constructed a Bayesian decoder to predict animals' behavior from pupil size and heart rate prior to stimulus presentation. The performance of the decoder was significantly better when using both heart rate and pupil size as inputs than when using either of them alone, suggesting the effects of the two arousal systems on behavior are not completely redundant. Supporting this notion, we found that, on a substantial portion of trials correctly predicted by the heart rate-based decoder, the pupil size-based decoder failed to correctly predict animals' behavior. Taken together, these results suggest that pupil-linked and heart rate-linked arousal systems exert different influences on animals' behavior.
Highlights
Behavioral state, including arousal and attention, profoundly influences brain functions underlying perception, cognition, and behavior (Castro-Alamancos and Connors, 1996; Cano et al, 2006; Niell and Stryker, 2010; McArthur and Dickman, 2011; McGinley et al, 2015a)
To understand the possible correlation between pupil-linked arousal and arousal indexed by electrocardiogram (ECG) signals, we trained 4 animals to perform a Go/No-go tactile discrimination task while simultaneously measuring their pupil size and ECG (Figure 1A)
We have previously reported a negative correlation between reaction time and pupil-linked arousal in rats performing tactile discrimination tasks (Schriver et al, 2018)
Summary
Behavioral state, including arousal and attention, profoundly influences brain functions underlying perception, cognition, and behavior (Castro-Alamancos and Connors, 1996; Cano et al, 2006; Niell and Stryker, 2010; McArthur and Dickman, 2011; McGinley et al, 2015a). It was shown that sensory responses were enhanced and population activity was less correlated in the high arousal state indicated by desynchronized membrane potentials (Reimer et al, 2014). Several physiological signals, including heart rate and pupil size have been used to index arousal, a state of physiological activation (Wekselblatt and Niell, 2015). Recent work has demonstrated that pupil size is able to track cortical state on a moment-by-moment basis (Reimer et al, 2014, 2016; McGinley et al, 2015a; Vinck et al, 2015), suggesting that pupil size is a peripheral index of an arousal system. The stimulation of the locus coeruleus—norepinephrine (LC-NE) system dilated the pupil, and improved the behavioral performance of rats performing perceptual tasks (Liu et al, 2017; Rodenkirch et al, 2019), indicating that pupil-linked arousal mediated by the LC-NE system modulates behavior
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