Influence of reward learning on visual attention and eye movements in a naturalistic environment: A virtual reality study

PLoS One. 2018 Dec 5;13(12):e0207990. doi: 10.1371/journal.pone.0207990. eCollection 2018.

Abstract

Rewards constitute crucial signals that motivate approach behavior and facilitate the perceptual processing of objects associated with favorable outcomes in past encounters. Reward-related influences on perception and attention have been reliably observed in studies where a reward is paired with a unidimensional low-level visual feature, such as the color or orientation of a line in visual search tasks. However, our environment is drastically different and composed of multidimensional and changing visual features, encountered in complex and dynamic scenes. Here, we designed an immersive virtual reality (VR) experiment using a 4-frame CAVE system to investigate the impact of rewards on attentional orienting and gaze patterns in a naturalistic and ecological environment. Forty-one healthy participants explored a virtual forest and responded to targets appearing on either the left or right side of their path. To test for reward-induced biases in spatial orienting, targets on one side were associated with high reward, whereas those on the opposite side were paired with a low reward. Eye-movements recording showed that left-side high rewards led to subsequent increase of eye gaze fixations towards this side of the path, but no such asymmetry was found after exposure to right-sided high rewards. A milder spatial bias was also observed after left-side high rewards during subsequent exploration of a virtual castle yard, but not during route turn choices along the forest path. Our results indicate that reward-related influences on attention and behavior may be better learned in left than right space, in line with a right hemisphere dominance, and could generalize to another environment to some extent, but not to spatial choices in another decision task, suggesting some domain- or context-specificity. This proof-of-concept study also outlines the advantages and the possible drawbacks of the use of the 3D CAVE immersive platform for VR in neuroscience.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Attention / physiology*
  • Cerebrum / anatomy & histology
  • Cerebrum / physiology
  • Female
  • Fixation, Ocular / physiology*
  • Functional Laterality / physiology
  • Humans
  • Learning / physiology*
  • Male
  • Orientation, Spatial / physiology*
  • Reward*
  • Space Perception / physiology*
  • Virtual Reality*

Grants and funding

This work was supported by grants from the Fondation Fyssen (AB); the Marie-Curie CoFund BRIDGE program (AB) from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement n° 267171"; the PRD of the University Hospital of Geneva; the National Center of Competence in Research (NCCR) for the Affective Sciences financed by the Swiss National Science Foundation (SNF No 51NF40-104897) and hosted by the University of Geneva; and an award from the Geneva Academic Society (Foremane Fund) to PV. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.