Abstract:Central to human and animal cognition is the ability to learn from feedback in order to optimize future rewards. Such a learning signal might be encoded and broadcasted by the brain’s arousal systems, including the noradrenergic locus coeruleus. Pupil responses and the P3 component of event-related potentials reflect rapid changes in the arousal level of the brain. Here we ask whether and how these variables may reflect “subjective surprise”: the mismatch between one’s expectation about being correct and the o… Show more
“…Changes in PS have been linked to uncertainty, from noise in integration processes 31 to confidence 32 , 33 and risk prediction errors or surprise. 6 , 7 , 8 , 34 In the foraging task, different levels of uncertainty can be achieved by varying the statistics of the environment (i.e., P REW and P DPL ). 25 In the easy protocol, where P REW and P DPL are high, site depletion most often happens early in the bout, and a few unrewarded licks are strong evidence in favor of site depletion.…”
Section: Resultsmentioning
confidence: 99%
“…In particular, the decreasing effects of photostimulation with increasing protocol uncertainty could be consistent with the hypothesis that 5-HT transients signal a prediction error 19 (here triggered artificially by photostimulation), a form of surprise reflected in transient pupil responses. 6 , 8 Figure 4 The Effects of DRN 5-HT Photostimulation Depend on the Level of Uncertainty (A–C) BPS, locomotor speed, and number of licks across protocols (mean ± SEM across sessions; low uncertainty, n = 29; medium uncertainty, n = 24; high uncertainty, n = 18). (D) Average change in PS of SERT-Cre mice between stimulated and non-stimulated bouts lasting at least 4 s, aligned to the first lick, and summary statistic (i.e., mean ± SEM across sessions of Δ PS estimated in a 0.5-s window, yellow).…”
Section: Resultsmentioning
confidence: 99%
“… Summary Transient variations in pupil size (PS) under constant luminance are coupled to rapid changes in arousal state, 1 , 2 , 3 which have been interpreted as vigilance, 4 salience, 5 or a surprise signal. 6 , 7 , 8 Neural control of such fluctuations presumably involves multiple brain regions 5 , 9 , 10 , 11 and neuromodulatory systems, 3 , 12 , 13 but it is often associated with phasic activity of the noradrenergic system. 9 , 12 , 14 , 15 Serotonin (5-HT), a neuromodulator also implicated in aspects of arousal 16 such as sleep-wake transitions, 17 motivational state regulation, 18 and signaling of unexpected events, 19 seems to affect PS, 20 , 21 , 22 , 23 , 24 but these effects have not been investigated in detail.…”
Summary
Transient variations in pupil size (PS) under constant luminance are coupled to rapid changes in arousal state,
1
,
2
,
3
which have been interpreted as vigilance,
4
salience,
5
or a surprise signal.
6
,
7
,
8
Neural control of such fluctuations presumably involves multiple brain regions
5
,
9
,
10
,
11
and neuromodulatory systems,
3
,
12
,
13
but it is often associated with phasic activity of the noradrenergic system.
9
,
12
,
14
,
15
Serotonin (5-HT), a neuromodulator also implicated in aspects of arousal
16
such as sleep-wake transitions,
17
motivational state regulation,
18
and signaling of unexpected events,
19
seems to affect PS,
20
,
21
,
22
,
23
,
24
but these effects have not been investigated in detail. Here we show that phasic 5-HT neuron stimulation causes transient PS changes. We used optogenetic activation of 5-HT neurons in the dorsal raphe nucleus (DRN) of head-fixed mice performing a foraging task. 5-HT-driven modulations of PS were maintained throughout the photostimulation period and sustained for a few seconds after the end of stimulation. We found no evidence that the increase in PS with activation of 5-HT neurons resulted from interactions of photostimulation with behavioral variables, such as locomotion or licking. Furthermore, we observed that the effect of 5-HT on PS depended on the level of environmental uncertainty, consistent with the idea that 5-HT could report a surprise signal.
19
These results advance our understanding of the neuromodulatory control of PS, revealing a tight relationship between phasic activation of 5-HT neurons and changes in PS.
“…Changes in PS have been linked to uncertainty, from noise in integration processes 31 to confidence 32 , 33 and risk prediction errors or surprise. 6 , 7 , 8 , 34 In the foraging task, different levels of uncertainty can be achieved by varying the statistics of the environment (i.e., P REW and P DPL ). 25 In the easy protocol, where P REW and P DPL are high, site depletion most often happens early in the bout, and a few unrewarded licks are strong evidence in favor of site depletion.…”
Section: Resultsmentioning
confidence: 99%
“…In particular, the decreasing effects of photostimulation with increasing protocol uncertainty could be consistent with the hypothesis that 5-HT transients signal a prediction error 19 (here triggered artificially by photostimulation), a form of surprise reflected in transient pupil responses. 6 , 8 Figure 4 The Effects of DRN 5-HT Photostimulation Depend on the Level of Uncertainty (A–C) BPS, locomotor speed, and number of licks across protocols (mean ± SEM across sessions; low uncertainty, n = 29; medium uncertainty, n = 24; high uncertainty, n = 18). (D) Average change in PS of SERT-Cre mice between stimulated and non-stimulated bouts lasting at least 4 s, aligned to the first lick, and summary statistic (i.e., mean ± SEM across sessions of Δ PS estimated in a 0.5-s window, yellow).…”
Section: Resultsmentioning
confidence: 99%
“… Summary Transient variations in pupil size (PS) under constant luminance are coupled to rapid changes in arousal state, 1 , 2 , 3 which have been interpreted as vigilance, 4 salience, 5 or a surprise signal. 6 , 7 , 8 Neural control of such fluctuations presumably involves multiple brain regions 5 , 9 , 10 , 11 and neuromodulatory systems, 3 , 12 , 13 but it is often associated with phasic activity of the noradrenergic system. 9 , 12 , 14 , 15 Serotonin (5-HT), a neuromodulator also implicated in aspects of arousal 16 such as sleep-wake transitions, 17 motivational state regulation, 18 and signaling of unexpected events, 19 seems to affect PS, 20 , 21 , 22 , 23 , 24 but these effects have not been investigated in detail.…”
Summary
Transient variations in pupil size (PS) under constant luminance are coupled to rapid changes in arousal state,
1
,
2
,
3
which have been interpreted as vigilance,
4
salience,
5
or a surprise signal.
6
,
7
,
8
Neural control of such fluctuations presumably involves multiple brain regions
5
,
9
,
10
,
11
and neuromodulatory systems,
3
,
12
,
13
but it is often associated with phasic activity of the noradrenergic system.
9
,
12
,
14
,
15
Serotonin (5-HT), a neuromodulator also implicated in aspects of arousal
16
such as sleep-wake transitions,
17
motivational state regulation,
18
and signaling of unexpected events,
19
seems to affect PS,
20
,
21
,
22
,
23
,
24
but these effects have not been investigated in detail. Here we show that phasic 5-HT neuron stimulation causes transient PS changes. We used optogenetic activation of 5-HT neurons in the dorsal raphe nucleus (DRN) of head-fixed mice performing a foraging task. 5-HT-driven modulations of PS were maintained throughout the photostimulation period and sustained for a few seconds after the end of stimulation. We found no evidence that the increase in PS with activation of 5-HT neurons resulted from interactions of photostimulation with behavioral variables, such as locomotion or licking. Furthermore, we observed that the effect of 5-HT on PS depended on the level of environmental uncertainty, consistent with the idea that 5-HT could report a surprise signal.
19
These results advance our understanding of the neuromodulatory control of PS, revealing a tight relationship between phasic activation of 5-HT neurons and changes in PS.
“…For instance, HRV has been linked to emotions 75 , stress 76 , attention 77 , empathy 6 and other cognitive factors 27 . Pupil dilation has been linked to arousal 78,79 , emotions 32,69 , effort 79,80 , surprise 31,81 , task engagement 38 , saliency 82 , attention 83 and more. As such, these measures are quite sensitive, but also quite unspecific.…”
Neural, physiological and behavioral signals synchronize between human subjects in a variety of settings. Multiple hypotheses have been proposed to explain this interpersonal synchrony, but there is no clarity under which conditions it arises, for which signals, or whether there is a common underlying mechanism. We hypothesized that similar cognitive processing of a shared stimulus is the source of interpersonal synchrony, measured here as inter-subject correlation. To test this we presented informative videos to participants in an attentive and distracted condition and subsequently measured information recall. Inter-subject correlation was observed for electro-encephalography, gaze position, pupil size and heart rate, but not respiration and head movements. The strength of correlation was co-modulated in the different signals, changed with attentional state, and predicted subsequent recall of information presented in the videos. There was robust within-subject coupling between brain, heart and eyes, but not respiration or head movements. The results suggest that inter-subject correlation is the result of similar cognitive processing and thus emerges only for those signals that exhibit a robust brain-body connection. While physiological and behavioral fluctuations may be driven by multiple features of the stimulus, correlation with other individuals is co-modulated by the level of attentional engagement with the stimulus.
“…However, a growing body of research shows that EEG measures are sensitive to prediction error during certain types of learning (Burnside, Fischer, & Ullsperger, 2019) and that arousal system responses are overall more predictive of surprise (de Gee et al, 2020), suggesting that the present findings cannot be explained by the limitations of EEG alone.…”
Associating a novel situation with a specific outcome involves a cascade of cognitive processes, including selecting relevant stimuli, forming predictions regarding expected outcomes, and updating memorized predictions based on experience. The present manuscript uses computational modeling and machine learning to test the hypothesis that alpha-band (8-12 Hz) neural oscillations are involved in the updating of expectations based on experience. Participants learned that a visual cue predicted an aversive loud noise with a probability of 50 percent. The Rescorla-Wagner model of associative learning explained trial-wise changes in self-reported noise expectancy as well as alpha power changes. Both experience in the past trial and self-reported expectancy for the subsequent trial were accurately decoded based on the topographical distribution of alpha power. Decodable information during initial association formation and contingency report recurred when viewing the conditioned cue. Findings support the idea that alpha oscillations have multiple, simultaneous, and unique roles in association formation.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
