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

Perceptual decision-making is a dynamic cognitive process and is shaped by many factors, including behavioral state, reward contingency, and sensory environment. To understand the extent to which adaptive behavior in decision-making is dependent on pupil-linked arousal, we trained head-fixed rats to perform perceptual decision-making tasks and systematically manipulated the probability of Go and No-go stimuli while simultaneously measuring their pupil size in the tasks. Our data demonstrated that the animals adaptively modified their behavior in response to the changes in the sensory environment. The response probability to both Go and No-go stimuli decreased as the probability of the Go stimulus being presented decreased. Analyses within the signal detection theory framework showed that while the animals' perceptual sensitivity was invariant, their decision criterion increased as the probability of the Go stimulus decreased. Simulation results indicated that the adaptive increase in the decision criterion will increase possible water rewards during the task. Moreover, the adaptive decision-making is dependent on pupil-linked arousal as the increase in the decision criterion was the largest during low pupil-linked arousal periods. Taken together, our results demonstrated that the rats were able to adjust their decision-making to maximize rewards in the tasks, and that adaptive behavior in perceptual decision-making is dependent on pupil-linked arousal.NEW & NOTEWORTHY Perceptual decision-making is a dynamic cognitive process and is shaped by many factors. However, the extent to which changes in sensory environment result in adaptive decision-making remains poorly understood. Our data provided new experimental evidence demonstrating that the rats were able to adaptively modify their decision criterion to maximize water reward in response to changes in the statistics of the sensory environment. Furthermore, the adaptive decision-making is dependent on pupil-linked arousal.

Multiple Transient Signals in Human Visual Cortex Associated with an Elementary Decision.

The cerebral cortex continuously undergoes changes in its state, which are manifested in transient modulations of the cortical power spectrum. Cortical state changes also occur at full wakefulness and during rapid cognitive acts, such as perceptual decisions. Previous studies found a global modulation of beta-band (12-30 Hz) activity in human and monkey visual cortex during an elementary visual decision: reporting the appearance or disappearance of salient visual targets surrounded by a distractor. The previous studies disentangled neither the motor action associated with behavioral report nor other secondary processes, such as arousal, from perceptual decision processing per se. Here, we used magnetoencephalography in humans to pinpoint the factors underlying the beta-band modulation. We found that disappearances of a salient target were associated with beta-band suppression, and target reappearances with beta-band enhancement. This was true for both overt behavioral reports (immediate button presses) and silent counting of the perceptual events. This finding indicates that the beta-band modulation was unrelated to the execution of the motor act associated with a behavioral report of the perceptual decision. Further, changes in pupil-linked arousal, fixational eye movements, or gamma-band responses were not necessary for the beta-band modulation. Together, our results suggest that the beta-band modulation was a top-down signal associated with the process of converting graded perceptual signals into a categorical format underlying flexible behavior. This signal may have been fed back from brain regions involved in decision processing to visual cortex, thus enforcing a "decision-consistent" cortical state.SIGNIFICANCE STATEMENT Elementary visual decisions are associated with a rapid state change in visual cortex, indexed by a modulation of neural activity in the beta-frequency range. Such decisions are also followed by other events that might affect the state of visual cortex, including the motor command associated with the report of the decision, an increase in pupil-linked arousal, fixational eye movements, and fluctuations in bottom-up sensory processing. Here, we ruled out the necessity of these events for the beta-band modulation of visual cortex. We propose that the modulation reflects a decision-related state change, which is induced by the conversion of graded perceptual signals into a categorical format underlying behavior. The resulting decision signal may be fed back to visual cortex.

Pupil-linked arousal modulates network-level EEG signatures of attention reorienting during immersive multitasking.

Objective. When multitasking, we must dynamically reorient our attention between different tasks. Attention reorienting is thought to arise through interactions of physiological arousal and brain-wide network dynamics. In this study, we investigated the relationship between pupil-linked arousal and electroencephalography (EEG) brain dynamics in a multitask driving paradigm conducted in virtual reality. We hypothesized that there would be an interaction between arousal and EEG dynamics and that this interaction would correlate with multitasking performance.Approach. We collected EEG and eye tracking data while subjects drove a motorcycle through a simulated city environment, with the instructions to count the number of target images they observed while avoiding crashing into a lead vehicle. The paradigm required the subjects to continuously reorient their attention between the two tasks. Subjects performed the paradigm under two conditions, one more difficult than the other.Main results. We found that task difficulty did not strongly correlate with pupil-linked arousal, and overall task performance increased as arousal level increased. A single-trial analysis revealed several interesting relationships between pupil-linked arousal and task-relevant EEG dynamics. Employing exact low-resolution electromagnetic tomography, we found that higher pupil-linked arousal led to greater EEG oscillatory activity, especially in regions associated with the dorsal attention network and ventral attention network (VAN). Consistent with our hypothesis, we found a relationship between EEG functional connectivity and pupil-linked arousal as a function of multitasking performance. Specifically, we found decreased functional connectivity between regions in the salience network (SN) and the VAN as pupil-linked arousal increased, suggesting that improved multitasking performance at high arousal levels may be due to a down-regulation in coupling between the VAN and the SN. Our results suggest that when multitasking, our brain rebalances arousal-based reorienting so that individual task demands can be met without prematurely reorienting to competing tasks.

Neuromodulation of Neural Oscillations in Health and Disease.

Using EEG and local field potentials (LFPs) as an index of large-scale neural activities, research has been able to associate neural oscillations in different frequency bands with markers of cognitive functions, goal-directed behavior, and various neurological disorders. While this gives us a glimpse into how neurons communicate throughout the brain, the causality of these synchronized network activities remains poorly understood. Moreover, the effect of the major neuromodulatory systems (e.g., noradrenergic, cholinergic, and dopaminergic) on brain oscillations has drawn much attention. More recent studies have suggested that cross-frequency coupling (CFC) is heavily responsible for mediating network-wide communication across subcortical and cortical brain structures, implicating the importance of neurotransmitters in shaping coordinated actions. By bringing to light the role each neuromodulatory system plays in regulating brain-wide neural oscillations, we hope to paint a clearer picture of the pivotal role neural oscillations play in a variety of cognitive functions and neurological disorders, and how neuromodulation techniques can be optimized as a means of controlling neural network dynamics. The aim of this review is to showcase the important role that neuromodulatory systems play in large-scale neural network dynamics, informing future studies to pay close attention to their involvement in specific features of neural oscillations and associated behaviors.

Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human.

Arousal levels perpetually rise and fall spontaneously. How markers of arousal-pupil size and frequency content of brain activity-relate to each other and influence behavior in humans is poorly understood. We simultaneously monitored magnetoencephalography and pupil in healthy volunteers at rest and during a visual perceptual decision-making task. Spontaneously varying pupil size correlates with power of brain activity in most frequency bands across large-scale resting state cortical networks. Pupil size recorded at prestimulus baseline correlates with subsequent shifts in detection bias (c) and sensitivity (d'). When dissociated from pupil-linked state, prestimulus spectral power of resting state networks still predicts perceptual behavior. Fast spontaneous pupil constriction and dilation correlate with large-scale brain activity as well but not perceptual behavior. Our results illuminate the relation between central and peripheral arousal markers and their respective roles in human perceptual decision-making.

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

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.

Interplay between components of pupil-linked phasic arousal and its role in driving behavioral choice in Go/No-Go perceptual decision-making.

In decision-making tasks, neural circuits involved in different aspects of information processing may activate the central arousal system, likely through their interconnection with brainstem arousal nuclei, collectively contributing to the observed pupil-linked phasic arousal. However, the individual components of the phasic arousal associated with different elements of information processing and their effects on behavior remain little known. In this study, we used machine learning techniques to decompose pupil-linked phasic arousal evoked by different components of information processing in rats performing a Go/No-Go perceptual decision-making task. We found that phasic arousal evoked by stimulus encoding was larger for the Go stimulus than the No-Go stimulus. For each session, the separation between distributions of phasic arousal evoked by the Go and by the No-Go stimulus was predictive of perceptual performance. The separation between distributions of decision-formation-evoked arousal on correct and incorrect trials was correlated with decision criterion but not perceptual performance. When a Go stimulus was presented, the action of go was primarily determined by the phasic arousal evoked by stimulus encoding. On the contrary, when a No-Go stimulus was presented, the action of go was determined by phasic arousal elicited by both stimulus encoding and decision formation. Drift diffusion modeling revealed that the four model parameters were better accounted for when phasic arousal elicited by both stimulus encoding and decision formation was considered. These results suggest that the interplay between phasic arousal evoked by both stimulus encoding and decision formation has important functional consequences on forming behavioral choice in perceptual decision-making.