Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes

Abstract

Declarative memories of personal experiences are a key factor in defining oneself as an individual, which becomes particularly evident when this capability is impaired. Assessing the physiological mechanisms of human declarative memory is typically restricted to patients with specific lesions and requires invasive brain access or functional imaging. We investigated whether the pupil, an accessible physiological measure, can be utilized to probe memories for complex natural visual scenes. During memory encoding, scenes that were later remembered elicited a stronger pupil constriction compared to scenes that were later forgotten. Thus, pupil size predicts success or failure of memory formation. In contrast, novel scenes elicited stronger pupil constriction than familiar scenes during retrieval. When viewing previously memorized scenes, those that were forgotten (misjudged as novel) still elicited stronger pupil constrictions than those correctly judged as familiar. Furthermore, pupil constriction was influenced more strongly if images were judged with high confidence. Thus, we propose that pupil constriction can serve as a marker of novelty. Since stimulus novelty modulates the efficacy of memory formation, our pupil measurements during learning indicate that the later forgotten images were perceived as less novel than the later remembered pictures. Taken together, our data provide evidence that pupil constriction is a physiological correlate of a neural novelty signal during formation and retrieval of declarative memories for complex, natural scenes.

Decision-related pupil dilation reflects upcoming choice and individual bias

“…More recent studies have linked pupil dilation to surprise about behaviorally relevant events (10,12,54), perceptual target detection (11,13), and report of transitions between percepts in bistable perceptual phenomena (6,14). Taken together, these findings establish that pupil dilation is a faithful reporter of the mental state of decision makers.…”

Subliminal Impending Collision Increases Perceived Object Size and Enhances Pupillary Light Reflex

“…However, recently a growing body of evidence has shown that the pupil not only constricts to physically bright object, but also to bright illusions (Laeng and Endestad, 2012), and even to imaginary bright situations (Laeng and Sulutvedt, 2014). Moreover, pupil constrictions as well respond to a variety of visual attributes besides brightness, including the inversion effect (Conway et al, 2008; Naber and Nakayama, 2013), novelty (Naber et al, 2013), conspecific faces (Conway et al, 2008; Ebitz et al, 2014), threatening animals (Naber et al, 2012), and the sun (Binda et al, 2013; Naber and Nakayama, 2013). The current study extends the scope of stimulus properties the pupil responds to, and demonstrates that it also constricts to subliminal threatening content conveyed by impending collision.…”

Pupil dilation during recognition memory: Isolating unexpected recognition from judgment uncertainty

“…This sample size was fixed with reference to prior pupillometry studies involving recognition memory (e.g. Naber et al, 2013;Otero et al, 2011).…”

“…The pupil is also sensitive to episodic memory judgments, dilating more for recognition probes identified as studied (old) versus unstudied (new) (Gardner, Mo, & Borrego, 1974;Heaver & Hutton, 2011;Naber, Frassle, Rutishauser, & Einhauser, 2013;Papesh, Goldinger, & Hout, 2012;Vo et al, 2008). As an extension of earlier work linking pupillary dilation to cognition (Beatty, 1982;Kahneman, 1973), this 'pupil old/new effect' has been suggested to reflect the increased 'cognitive load' or voluntary effort required during the successful retrieval of episodic content.…”