Perceptual Behavior Depends Differently on Pupil-Linked Arousal and Heartbeat Dynamics-Linked Arousal in Rats Performing Tactile Discrimination Tasks

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.

The Neuromodulatory Role of the Noradrenergic and Cholinergic Systems and Their Interplay in Cognitive Functions: A Focused Review

“…More recent work, however, has also highlighted the role of ACh in attentional effort, orienting, and the detection of behaviorally significant stimuli [ 17 , 18 ]. Norepinephrine (NE) has classically been viewed as a major mediator of arousal that plays an important role in regulating the efficiency of external sensory processing [ 19 , 20 , 21 , 22 , 23 , 24 , 25 ]. Recent work expanding on this has revealed a varied and complex role for the noradrenergic system in everything from memory formation [ 26 ] to executive function and attention [ 27 , 28 ], to cognitive flexibility [ 29 , 30 ], and to decision-making [ 31 , 32 , 33 ].…”

Rapid Effects of Vagus Nerve Stimulation on Sensory Processing Through Activation of Neuromodulatory Systems

“…Sensory processing is highly dependent upon behavioral states such as attention and arousal ( Nicolelis and Fanselow, 2002 ; Carrasco et al, 2004 ; Niell and Stryker, 2010 ; Bennett et al, 2013 ; Reimer et al, 2014 , 2016 ; McGinley et al, 2015 ; Vinck et al, 2015 ; Zheng et al, 2015 ; Schriver et al, 2018 , 2020 ; Liu et al, 2021 ) as both are heavily influenced by the same global neuromodulatory systems, including the noradrenergic ( Berridge and Waterhouse, 2003 ; Aston-Jones and Waterhouse, 2016 ; Liu et al, 2017 ; Chandler et al, 2019 ) and cholinergic systems ( Pinto et al, 2013 ). For example, our laboratory recently demonstrated that activation of the locus coeruleus – norepinephrine system (LC-NE), a major neuromodulator of attention and arousal, rapidly enhanced somatosensory processing through NE-mediated suppression of burst spiking induced by calcium T-type channels ( Rodenkirch et al, 2019 ).…”

Adaptive decision making depends on pupil-linked arousal in rats performing tactile discrimination tasks

“…Buprenorphine (Buprenex, 0.03 mg/kg, SC) was administered as an analgesic and Ringers solution (2 mL, SC) was also administered to prevent dehydration. After exposing and cleaning the skull, 8-10 burr holes were drilled in the skull, and stainless steel screws (0-80 thread, McMaster Carr, Robbinsville, NJ) were inserted to anchor a head-plate (Bari et al, 2013; Liu et al, 2021). The wound was then closed with surgical sutures and treated with antibiotic ointment.…”

“…Training and the Go/No-go Discrimination Task. Water deprivation schedule and procedures of head-fixation habituation were the same as our previous work (Schriver et al, 2018;Schriver et al, 2020;Liu et al, 2021). Briefly, restriction of access to water was used to motivate animals during the tasks.…”

“…In perceptual decision making tasks, sensory information is accumulated over time in the central nervous system, eventually leading to a decision to choose one of the alternatives and generating motor commands to indicate the animal’s choice (Smith and Ratcliff, 2004; Gold and Shadlen, 2007; Carandini and Churchland, 2013; Brody and Hanks, 2016; Schriver et al, 2020). The perceptual decision making process is shaped by many factors, including brain state, the gain/loss of each possible decision, task engagement, and external sensory environment (Murphy et al, 2014; Lee and Margolis, 2016; de Gee et al, 2017; Schriver et al, 2018; Cardoso et al, 2019; Kloosterman et al, 2019; Stolyarova et al, 2019; de Gee et al, 2020; Monosov, 2020; Liu et al, 2021; Ashwood et al, 2022). For example, Waiblinger et al (2019) reported that, in a tactile detection task, rats adjusted their behavioral strategy to maintain a constant payoff in response to changes in probabilistic distribution of whisker deflection amplitudes.…”