Ocular measures during associative learning predict recall accuracy

Abstract

The ability to form associations between stimuli and commit those associations to memory is a cornerstone of human cognition. Dopamine and noradrenaline are critical neuromodulators implicated in a range of cognitive functions, including learning and memory. Eye blink rate (EBR) and pupil diameter have been shown to index dopaminergic and noradrenergic activity. Here, we examined how these ocular measures relate to accuracy in a paired-associate learning task where participants (N = 73) learned consistent object-location associations over eight trials consisting of pre-trial fixation, encoding, delay, and retrieval epochs. In order to examine how within-subject changes and between-subject changes in ocular metrics related to accuracy, we mean centered individual metric values on each trial based on within-person and across-subject means for each epoch. Within-participant variation in EBR was positively related to accuracy in both encoding and delay epochs: faster EBR within the individual predicted better retrieval. Differences in EBR across participants was negatively related to accuracy in the encoding epoch and in early trials of the pre-trial fixation: faster EBR, relative to other subjects, predicted poorer retrieval. Visual scanning behavior in pre-trial fixation and delay epochs was also positively related to accuracy in early trials: more scanning predicted better retrieval. We found no relationship between pupil diameter and accuracy. These results provide novel evidence supporting the utility of ocular metrics in illuminating cognitive and neurobiological mechanisms of paired-associate learning.

Keywords: Associative learning; Eye blink; Memory; Pupil.

Figure 1.. Associative Learning and Memory Paradigm.

(a) Schematic illustration portraying the trial structure, which consists of four discrete epochs, each 27s in duration: fixation, encoding, delay, and retrieval. During the encoding epoch, nine stimuli (e.g. pen, shoe) were sequentially presented for 3s in each location on the grid. During the retrieval epoch, participants were cued by a filled-square to verbalize their response at each location. There were eight total learning trials (b) Nine equi-familiar stimuli were shown during the encoding epoch of each of the 8 learning trials. The white number in the corner of the cell represents the order at which these stimuli were presented within a given learning trial. Object-location pairings remained consistent across trials; however, the sequence was pseudorandomized by trial and consistent across participants.

Figure 2.. Associative learning performance.

Mean percentage of correct responses per learning trial fitted by a negatively accelerated learning function.

Figure 3.

Pupil diameter (A) and eye blink rate (B) across learning trials and averaged across participants for each analyzed epoch.

Figure 4.

Significant fixed effects and their interaction with time for within-person mean centered EBR (top row), grand-mean centered EBR (middle row), and distance between fixations (bottom row). Estimates for main effects are indicated with a subscripted m and estimates for interactions with trial are indicated with a subscripted i.