Scene-based contextual cueing in pigeons.

The environment is replete with visual information. At any given time, people must attend to relevant stimuli and ignore irrelevant stimuli in order to engage in adaptive behavior. For example, to safely cross the street, we attend to the color of the traffic lights as well as to the motion of nearby cars and pedestrians, while we simultaneously ignore the buildings and trees along the roadway. Salient visual objects can unconditionally command our attention (Awh, Belopolsky, & Theeuwes, 2012). Yet, such “bottom-up” control may not tell the full story of how we navigate the complex visual contexts that we confront in everyday life; experience-dependent “top-down” control may also play a key part in behavioral adaptation (Chun, 2000). For instance, should we be looking for a pharmacy in France, we would do well to peer above the doorways where a green cross is most likely to be displayed; but, should we be seeking a street sign, we would best be advised to gaze toward corner buildings where road placards are most likely to be affixed. The significance of context to visual object identification has long been appreciated (e.g., Biederman, 1972). Still more recent research by Chun and Jiang (1998) initiated a new chapter on the importance of contextual stimuli to adaptive visual behavior. These investigators discovered that the spatial configuration of objects in a visual scene can serve as a powerful contextual cue, facilitating an individual's search for a target item. Specifically, Chun and Jiang found that, when the specific location of a target was consistently associated with a particular spatial arrangement of distractor items in the display, reaction times (RTs) to identify the target became reliably shorter than when the target appeared in newly generated spatial arrangements of the same distractor items. Chun and Jiang called this RT benefit the contextual cueing effect and proposed that contextual cueing is due to attention being guided toward the location of the target, owing to learned associations between the context and the location of the target. Subsequent research has sought to elucidate the perceptual and cognitive mechanisms underlying contextual cueing in humans. Possible animal models of contextual cueing have only recently been developed (for pigeons: Brooks, Rasmussen, Hollingworth, & Wasserman, 2008; for rhesus monkeys: Brooks, Dai, & Sheinberg, 2011), with the recent paper by Goujon and Fagot (2013: for baboons) being the first published demonstration. Here, we report the results of a new pigeon analog of the human contextual cueing task in the hope of shedding fresh light on the comparative and associative mechanisms underlying contextual cueing. Chun (2000) offered two compelling justifications for the comparative study of contextual cueing. First, most research in visual processing gives little consideration to the history of the observer; being endowed with the capacity to see also requires that organisms learn to interpret their visual world based on their experience in it. Second, more needs to be understood concerning the neural mechanisms and evolutionary origins of attentional guidance. For these reasons, animal models are critical for controlling and isolating the role of learning in contextual cueing as well as for elucidating its physiological and phylogenetic foundations (Lazareva, Shimizu, & Wasserman, 2012). A critical feature of our present project was that it used photographs of real scenes as experimental contexts. Although contextual cueing has been demonstrated in humans using both naturalistic scenes and arrays of abstract distractors (e.g., Brockmole & Henderson, 2006a; Brockmole & Henderson, 2006b; Rosenbaum & Jiang, 2013), experiments have consistently shown that lifelike scene-target associations are learned faster and more strongly contribute to search time benefits than do distractor array-target associations. Thus, we used color photographs of real-world scenes in order to maximize the effect of contextual cueing on pigeons' visually guided behavior. We also investigated the time between context and target presentation (Stimulus Onset Asynchrony, SOA) from 0 s to 8 s to see if different SOAs differentially affect contextual cueing. In most human studies of contextual cueing, the context and target are simultaneously presented. Only a few studies have programmed a nonzero SOA between context and target presentation, ranging from 250 ms to 1,500 ms (Geyer, Zehetleitner, & Muller, 2010; Goujon, 2011; Jiang, Sigstad, & Swallow, 2013; Kunar, Flusberg, & Wolfe, 2006, 2008; Ogawa & Kumada, 2008; Peterson, & Kramer, 2001). Even fewer studies have parametrically investigated the effect of the SOA on contextual cueing. Kunar et al. (2006) found a slight weakening of contextual cueing with increasing SOAs and Kunar et al. (2008) observed a more robust SOA effect when placeholders demarcated the possible target locations. More recently, Jiang et al. (2012) reported that contextual cueing was similar across SOAs from 0 ms to 1,000 ms. This manipulation of SOA also afforded us the ability to explore the possible role of attentional guidance by closely monitoring the pigeons' behavior during the 1 s to 8 s prior to the presentation of the target. Here, we leveraged the fact that pigeons will make unsolicited anticipatory reports in the location of impending stimuli that predict reward (Brooks, 2010), which can be used as an on-line measure of attentional guidance similar to the use of eye and hand movements in human subjects (see Peterson & Kramer, 2001; Spivey 2008). In overview, the present project used photographs of real-world scenes to explore contextual cueing and its possible mechanisms in pigeons. In Experiments 1 and 2, we gave the same experimental procedures to two different sets of birds in different orders. On half of the daily trials, each of four scenes perfectly predicted the target's location (Predictive condition); on the other half of the trials, none of four other scenes predicted the target's location, with the target randomly appearing in one of the same four possible locations (Random condition). Evidence of contextual cueing would come from shorter RTs in the Predictive condition than in the Random condition. Furthermore, we manipulated the temporal delay between presentations of the contextual stimuli and the target stimuli to see what effect this delay would have on contextual cueing. We also monitored pecking during the delay to see if such anticipatory responding provided any clues as to the associative nature of contextual cueing. Finally, in Experiment 3, we vertically and horizontally reversed the Predictive photographic scenes to see whether the global scene contexts and/or the local cues in the immediate vicinity of the upcoming target exerted greater control over pigeons' visually directed responding. Assessing the contributions of global and local cues has been a topic of considerable interest to researchers studying animal spatial cognition (Brown & Cook, 2006).