Pupil-linked arousal modulates behavior in rats performing a whisker deflection direction discrimination task

Schriver, Brian J.; Bagdasarov, Svetlana; Wang, Qi

doi:10.1152/jn.00290.2018

Cited by 49 publications

(75 citation statements)

References 90 publications

(130 reference statements)

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“…First, we show that tonic, baseline pupil size depends on the speed‐accuracy trade‐off set by the participant per trial. These effects are in line with previous findings by studies with humans (Murphy, Boonstra, et al, ; Naber et al, ) and rodents (Schriver, Bagdasarov, & Wang, ) and suggest that the pupil's sensitivity adjustments in the speed‐accuracy trade‐off is not limited to a specific task context. Aside from this finding, several other aspects of our results warrant further consideration.…”

Section: Discussionsupporting

confidence: 91%

Pupillometric investigation into the speed‐accuracy trade‐off in a visuo‐motor aiming task

Naber

Murphy

2019

Psychophysiology

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Convergent lines of evidence suggest that fluctuations in the size of the pupil may be associated with the trade‐off between the speed (adrenergic, sympathetic) and accuracy (cholinergic, parasympathetic) of behavior across a variety of task contexts. Here, we explored whether pupil size was related to this trade‐off during a visuospatial motor aiming task. Participants were shown visual targets at random locations on a screen and were instructed and incentivized to move a computer mouse‐controlled cursor to the center of the targets, either as fast as possible, as accurately as possible, or to strike a balance between the two. Behavioral results showed that these instructions led to typical speed‐accuracy trade‐off effects on movement reaction times and hit distances to target centers. Pupillometric analyses revealed that movements were faster and less accurate when participants had relatively large baseline pupil sizes, as measured before target onset. Furthermore, trial‐evoked pupil dilation was related specifically to a bias toward speed in the trade‐off and the speed of the ballistic and error‐correction phases of the motor responses such that larger pupils predicted shorter latencies and higher movement speeds. Pupil responses were also associated with performance in a manner that may reflect the combined influence of a number of factors, including the generation of dynamic urgency and an arousal response to negative feedback. Our results generally support a role for pupil‐linked arousal in regulating the trade‐off between speed and accuracy, while also highlighting how the trial‐related pupil response can exhibit multifaceted, temporally discrete associations with behavior.

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Section: Discussionsupporting

confidence: 91%

Pupillometric investigation into the speed‐accuracy trade‐off in a visuo‐motor aiming task

Naber

Murphy

2019

Psychophysiology

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“…This result supports the model that phasic neuromodulatory signals that occur naturally are strongest during intermediate levels of tonic neuromodulatory activity (Aston-Jones and Cohen, 2005). This model is further supported by recent observations that tonic arousal predicts nonmonotonic (inverted U) changes in the signal-to-noise ratio of sensory cortical responses and perceptual sensitivity (McGinley et al, 2015a;Schriver et al, 2018;Waschke et al, 2019). Note that we observed the inverted U relationship after correcting for a general reversion to mean.…”

Section: Discussionsupporting

confidence: 90%

Graded recruitment of pupil-linked neuromodulation by parametric stimulation of the vagus nerve

Mridha

Gee

Shi

et al. 2019

Preprint

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Vagus nerve stimulation (VNS) is thought to alter the state of the brain by recruiting global neuromodulators. VNS is used in treatment-resistant epilepsy, and is increasingly being explored for other brain disorders, such as depression, and as a cognitive enhancer. However, the promise of VNS is only partially fulfilled due to a lack of mechanistic understanding of the transfer function between stimulation parameters and neuromodulatory response, together with a lack of biosensor for assaying stimulation efficacy in real time. We here develop an approach to VNS in head-fixed mice on a treadmill, and use it to show that pupil dilation is a biosensor for VNS-evoked cortical neuromodulation. In a 'goldilocks' zone of stimulation parameters, current leakage and off-target effects are minimized and the extent of pupil dilation tracks VNS-evoked basal-forebrain cholinergic axon activity in auditory cortex. Thus, pupil dilation is a sensitive readout of the moment-by-moment titratable effects of VNS on brain state.

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“…However, the accumulating evidence suggests that perceptual decision is also significantly affected by latent subjective states reflecting task engagement 8 . For instance, behavioral response variability is correlated with mind wondering in humans 9 and fluctuations of physiological and behavioral states in animals [10][11][12][13] . These drifts of subjective states could be partially attributed to the fluctuation of cortical states [13][14][15] .…”

Section: Introductionmentioning

confidence: 99%

Visually-evoked choice behavior driven by distinct population computations with non-sensory neurons in visual cortical areas

Osako

Ohnuki

Tanisumi

et al. 2020

Preprint

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During visual detection tasks, subjects sometimes fail to respond to identical visual stimuli even when the stimuli are registered on their retinas. It is widely assumed that variability in detection performance is attributed to the fidelity of the visual responses in visual cortical areas, which could be modulated by fluctuations of subjective internal states such as vigilance, attention, and reward experiences. However, it is not clear what neural ensembles represent such different internal states. Here, we utilized a behavioral task that differentiated distinct perceptual states to identical stimuli, and analyzed neuronal responses simultaneously recorded from both primary visual cortex (V1) and posterior parietal cortex (PPC) during the task. We found that population activity differed across choice types with the major contribution of non-sensory neurons, rather than visually-responsive neurons, in V1 as well as PPC. The distinct population-level activity in V1, but not PPC, was restricted within the stimulus presentation epoch, which was distinguished from pre-stimulus background activity and was supported by near-zero noise correlation. These results indicate a major contribution of non-sensory neurons in V1 for population-level computation that enables behavioral responses from visual information.2 instance, in sensory detection task, human or animal subjects are instructed or well-trained to 3 reliably report the presence and absence of sensory stimuli to obtain rewards. When the sensory 4 evidence is near threshold for the decision criterion, the subjects' reports vary across trials 5 despite the best efforts of subjects to get rewards. Interestingly, even if they report the absence 6 of stimuli, it is sometimes possible that they could correctly guess the contents of the stimuli 7 above chance level if they are forced to answer 1-8 . Revealing the neural mechanisms underlying 8 such trial-by-trial variability of perceptual reports is crucial to understand how the brain exploits 9 sensory information for optimal decision making. 11The trial-by-trial variance of the responses to identical stimuli is believed to reflect noises in 12 conversion of sensory information into motor outputs 9 . It has been demonstrated that variability 13 of firing rates of sensory neurons is responsible for the trial-by-trial variability of choices 10-14 .14 However, the accumulating evidence suggests that perceptual decision is also significantly 15 affected by latent subjective states reflecting task engagement 15,16 . For instance, it is known that 16 behavioral response variability is correlated with mind wondering in humans 17 and fluctuations 17 of physiological and behavioral states in animals [18][19][20][21][22] . These drifts of subjective states could be 18 partially attributed to fluctuation of cortical states 22-28 , in which synchronization and 19 desynchronization of many neurons in particular areas of cortex could affect efficiency of the 20 population coding 29,30 . In addition, the task engagement is known t...

show abstract

Pupil-linked arousal modulates behavior in rats performing a whisker deflection direction discrimination task

Cited by 49 publications

References 90 publications

Pupillometric investigation into the speed‐accuracy trade‐off in a visuo‐motor aiming task

Pupillometric investigation into the speed‐accuracy trade‐off in a visuo‐motor aiming task

Graded recruitment of pupil-linked neuromodulation by parametric stimulation of the vagus nerve

Visually-evoked choice behavior driven by distinct population computations with non-sensory neurons in visual cortical areas

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