Pupil size reflects successful encoding and recall of memory in humans

Pupil responses are known to indicate brain processes involved in perception, attention and decision-making. They can provide an accessible biomarker of human memory performance and cognitive states in general. Here we investigated changes in the pupil size during encoding and recall of word lists. Consistent patterns in the pupil response were found across and within distinct phases of the free recall task. The pupil was most constricted in the initial fixation phase and was gradually more dilated through the subsequent encoding, distractor and recall phases of the task, as the word items were maintained in memory. Within the final recall phase, retrieving memory for individual words was associated with pupil dilation in absence of visual stimulation. Words that were successfully recalled showed significant differences in pupil response during their encoding compared to those that were forgotten – the pupil was more constricted before and more dilated after the onset of word presentation. Our results suggest pupil size as a potential biomarker for probing and modulation of memory processing.

[1]  Stephen V. David,et al.  Cortical Membrane Potential Signature of Optimal States for Sensory Signal Detection , 2015, Neuron.

[2]  G. Repovš,et al.  Fine-grained versus categorical: Pupil size differentiates between strategies for spatial working memory performance. , 2017, Psychophysiology.

[3]  Ueli Rutishauser,et al.  Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes. , 2013, Journal of vision.

[4]  D. McCormick Cholinergic and noradrenergic modulation of thalamocortical processing , 1989, Trends in Neurosciences.

[5]  Christof Koch,et al.  Fully Formatted Pdf and Full Text (html) Versions Will Be Made Available Soon. Pupil Dilation Betrays the Timing of Decisions , 2022 .

[6]  V. Fabian,et al.  41. Application of eye tracking in neuroscience , 2015, Clinical Neurophysiology.

[7]  Michael J. Kahana,et al.  Foundations of Human Memory , 2012 .

[8]  C. Koch,et al.  Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry , 2008, Proceedings of the National Academy of Sciences.

[9]  Hongkeun Kim,et al.  Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies , 2011, NeuroImage.

[10]  Brent M. Berry,et al.  Dissecting gamma frequency activity during human memory processing , 2017, Brain : a journal of neurology.

[11]  Michael J. Jutras,et al.  Direct Brain Stimulation Modulates Encoding States and Memory Performance in Humans , 2017, Current Biology.

[12]  Mark R. Bower,et al.  High frequency oscillations are associated with cognitive processing in human recognition memory. , 2014, Brain : a journal of neurology.

[13]  M. Kahana The Cognitive Correlates of Human Brain Oscillations , 2006, The Journal of Neuroscience.

[14]  Thilo Womelsdorf,et al.  Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus , 2015, The Journal of Neuroscience.

[15]  E. Hess,et al.  Pupil Size as Related to Interest Value of Visual Stimuli , 1960, Science.

[16]  D. McCormick,et al.  Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex , 2016, Nature Communications.

[17]  D Kahneman,et al.  Pupil Diameter and Load on Memory , 1966, Science.

[18]  Michael J. Jutras,et al.  Oscillatory activity in the monkey hippocampus during visual exploration and memory formation , 2013, Proceedings of the National Academy of Sciences.

[19]  J. Diamond,et al.  Sclerotomy complications following pars plana vitrectomy , 2000, The British journal of ophthalmology.

[20]  E. Hess,et al.  Pupil Size in Relation to Mental Activity during Simple Problem-Solving , 1964, Science.

[21]  S. Hutton,et al.  Keeping an eye on the truth? Pupil size changes associated with recognition memory , 2011, Memory.

[22]  A. Jacobs,et al.  The coupling of emotion and cognition in the eye: introducing the pupil old/new effect. , 2007, Psychophysiology.

[23]  J. M. Lina,et al.  Recording and analysis techniques for high-frequency oscillations , 2012, Progress in Neurobiology.

[24]  S. Hutton,et al.  Pupil size changes during recognition memory. , 2011, Psychophysiology.

[25]  George H. Denfield,et al.  Pupil Fluctuations Track Fast Switching of Cortical States during Quiet Wakefulness , 2014, Neuron.

[26]  Kari L. Hoffman,et al.  Sharp-Wave Ripples in Primates Are Enhanced near Remembered Visual Objects , 2017, Current Biology.

[27]  Nicole M. Long,et al.  Human intracranial high-frequency activity maps episodic memory formation in space and time , 2014, NeuroImage.