Ecological Origins of Object Salience: Reward, Uncertainty, Aversiveness, and Novelty.

Okihide Hikosaka,Ali Ghazizadeh,Whitney Griggs

doi:10.3389/fnins.2016.00378

Abstract

Among many objects around us, some are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), while others may become salient by virtue of their ecological relevance through experience. However, the role of ecological experience in automatic attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (>300), each experienced repeatedly (>5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e., positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g., airpuff), but negative for others (e.g., time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such high capacity for learned salience, the ability to rapidly choose important objects can grow during the entire life to promote biological fitness.

Highlights

Attention can be used to actively search for and focus on something important
Previous studies in our laboratory suggest that changing object salience may require multiple days (>5 days) of training and may rely on different neural mechanisms compared with short-term flexible object outcome pairing (Yasuda et al, 2012; Kim and Hikosaka, 2013; Kim et al, 2015)
The results indicate that uncertain objects had higher salience [Figure 4G, main effect of uncertainty F(2, 114) > 4.1, P < 0.05] in all subjects (Figure 4H, positive slopes), the effect was unclear between the two high levels of uncertainty (0.18 vs. 0.25)

Summary

Introduction

Attention can be used to actively search for and focus on something important (top-down attention). Attention is automatically attracted to delicious foods (Nijs et al, 2010), erotic images (Lykins et al, 2006), faces (Hershler and Hochstein, 2005; Theeuwes and Van Der Stigchel, 2006), emotional expressions (Mogg and Bradley, 1999), and feared animals (Ohman et al, 2001), which represent ecological features. In such cases, the origin of salience (i.e., attentional bias) is often unclear. In order to reveal the neural mechanisms of salience, it is critical to dissociate the different origins experimentally

Methods

Results

Conclusion