Pupillary Dilations of Mice Performing a Vibrotactile Discrimination Task Reflect Task Engagement and Response Confidence

Dan Alin Ganea; Alexander Bexter; Mathias Günther; Pierre-Marie Gardères; Björn M Kampa; Florent Haiss

doi:10.3389/fnbeh.2020.00159

Pupillary Dilations of Mice Performing a Vibrotactile Discrimination Task Reflect Task Engagement and Response Confidence

Front Behav Neurosci. 2020 Sep 3:14:159. doi: 10.3389/fnbeh.2020.00159. eCollection 2020.

Authors

Dan Alin Ganea^{1

2

3}, Alexander Bexter^{4

5}, Mathias Günther^{1

2

3}, Pierre-Marie Gardères^{1

2

3

6}, Björn M Kampa^{4

5

7}, Florent Haiss^{1

2

3

6}

Affiliations

¹ IZKF, Medical Faculty, RWTH Aachen University, Aachen, Germany.
² Institute of Neuropathology, RWTH Aachen University, Aachen, Germany.
³ Department of Ophthalmology, RWTH Aachen University, Aachen, Germany.
⁴ Department of Neurophysiology, Institute of Zoology, RWTH Aachen University, Aachen, Germany.
⁵ Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, Aachen, Germany.
⁶ Unit of Neural Circuits Dynamics and Decision Making, Institut Pasteur, Paris, France.
⁷ JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Jülich Forschungszentrum, Jülich, Germany.

Abstract

Pupillometry, the measure of pupil size and reactivity, has been widely used to assess cognitive processes. Changes in pupil size have been shown to correlate with various behavioral states, both externally and internally induced such as locomotion, arousal, cortical state, and decision-making processes. Besides, these pupillary responses have also been linked to the activity of neuromodulatory systems that modulate attention and perception such as the noradrenergic and cholinergic systems. Due to the extent of processes the pupil reflects, we aimed at further resolving pupillary responses in the context of behavioral state and task performance while recording pupillary transients of mice performing a vibrotactile two-alternative forced-choice task (2-AFC). We show that before the presentation of task-relevant information, pre-stimulus, pupil size differentiates between states of disengagement from task performance vs. engagement. Also, when subjects have to attend to task stimuli to attain a reward, post-stimulus, pupillary dilations exhibit a difference between correct and error responses with this difference reflecting an internal decision variable. We hypothesize that this internal decision variable relates to response confidence, the internal perception of the confidence the subject has in its choice. As opposed to this, we show that in a condition of passive performance, when the stimulus has no more task relevance due to reward being provided automatically, pupillary dilations reflect the occurrence of stimulation and reward provision but not decisional variables as under active performance. Our results provide evidence that in addition to reflecting attentiveness under task performance rather than arousal per se, pupil dilations also reflect the confidence of the subject in his ensuing response. This confidence coding is overlaid within a more pronounced pupil dilation that reflects post-decision components that are related to the response itself but not to the decision. We also provide evidence as to how different behavioral states, imposed by task demands, modulate what the pupil is reflecting, presumably showing what the underlying cognitive network is coding for.

Keywords: 2-AFC; arousal; confidence representation; decision making; locomotion; pupillometry; somatosensory discrimination.