Direct Eye Gaze May Represent a “Special Class” of

The social stimuli utilized in the Social Target Detection Task were images of neutral eyes with direct gaze. The knowledge that eyes are the most attended component of faces formed the basis of the decision to focus on the eyes, as opposed to whole face stimuli. Preferential attention to the eye region of faces has been demonstrated in a number of non-human primates and a similar preference has been identified in human infants as young as two month of age (Emery, 2000; Farroni et al., 2004). In addition to identifying the presence or absence of eyes in a stimulus, the ability to determine whether gaze is directed towards or away from the viewer is also conserved across many species. It is suggested that this ability is innate based on the evolutionary importance of this distinction in prey species for which direct gaze is a very different threat cue than averted gaze (Emery, 2000).

communicative information that is equally important. Thus, the evolution of the human eye is suggested to have evolved specifically to promote the transfer of communicative information based on the direction of gaze (Emery, 2000). Evidence that, even as compared to our closest non-human primate cousins, human eyes have the largest ratio of white (sclera) to dark (iris) area supports this. This increased contrast in the eyes allows for easier and more quick discrimination of the direction of gaze based on how much of the white sclera is visible (Emery, 2000). Humans are equipped with the ability to quickly analyze visual input for social relevance and to preferentially attend to direct gaze from birth. Furthermore, this process is likely facilitated by the salient sclera to iris ratio of the human eye (Farroni et al., 2002; Itier and Batty, 2009). Additionally, behavioral studies have shown that in neurotypical children and adolescents, detection of a target face is facilitated when the face has direct as opposed to averted gaze (Macrae et al., 2002; Senju et al., 2003; von Grunau and Anston, 1995). Together, this suggests that eyes, particularly eyes with gaze directed at the observer, likely comprise a “special” stimulus class that captures attention and may be subject to preferential processing. Indeed, direct gaze activates the brain’s arousal system resulting in a reorientation of attention that enhances social processing and modulates ongoing and subsequent perceptual and cognitive processes (Engell et al., 2010; Senju and Hasegawa, 2005; Senju and Johnson, 2009). The ability of direct gaze to enhance social and cognitive processing, including facilitating the encoding and recognition of faces, has been demonstrated in infants as young as four months old (Farroni et al., 2002; Farroni et al., 2004; Farroni et al., 2007). Furthermore, direct gaze has been

shown to not only capture attention, but to also increase attention dwell time, delaying disengagement and enhancing processing of stimuli (George and Conty, 2008; Senju and Hasegawa, 2005). Therefore, based on behavioral findings, it is likely that the use of direct gaze stimuli in the current task enhanced attentional processing of the target stimuli in neurotypical controls.

In an effort to promote the interaction between the eye distracter and the target, the target was positioned directly between the eyes in the Target Eyes condition. It has been shown that when target and distracter stimuli are presented in the same receptive field, such as in the Target Eyes condition, the entire stimulus object is processed in parallel before individual components are separated for further processing (Desimone and Duncan, 1995; Pessoa et al., 2002a). Thus, because direct gaze stimuli modulate both cognition and attention, it is possible that combining the target with direct gaze enhanced the parallel processing of both the distracter eyes and the target. Increased accuracy to the Target Eyes as compared to when the target was presented alone suggests that this may be the case. The finding that reaction time (RT) was equivalent between these two conditions suggests that, while the eyes did enhance processing of the target stimulus, it was not likely due to the target being more readily perceivable when overlaid on the eyes. The similar reaction time further suggests that it is unlikely that the Target Eye condition was more salient than when the target was presented alone. If either of those were the case, then we would have expected faster RTs in the Target Eyes condition. Instead, it is likely that the equivalent reaction time to both the Target Alone and the Target Eyes represents the time it takes to make a behavioral switch

to a novel motor response, as opposed to being associated with attentional or target detection processes. Together this suggests that the presence of neutral eyes with direct gaze in a subset of trials resulted in the enhanced processing of those stimuli and this facilitated target detection when pairing the eyes with the target.

As previously highlighted, both top-down task-related cognitive control mechanisms and bottom-up sensory driven information are engaged and exert influence on selective attention when processing novel stimuli. However, when there is a need to overcome competition by task-irrelevant stimuli, attentional top- down feedback processes are engaged to a greater degree in order to overcome the bottom-up responses and facilitate the processing of the goal-relevant aspects of the stimulus (Corbetta and Shulman, 2002; Pessoa et al., 2002a). Therefore, it is likely that in the current paradigm top-down attentional resources were engaged in an effort to resolve the competition between the goal-directed processing of the target and the bottom-up influence of the salient direct gaze stimulus. Indeed, it has been shown that top-down feedback processes can bias the focus of attention away from salient distracters in favor of neural networks involved in processing the stimulus attributes that are most likely to facilitate goal-direct processes (Kastner and Ungerleider, 2000). Thus, while the target and distracter stimuli were initially processed in parallel, it is likely that there was subsequent recruitment of top-down attention mechanisms to enhance processing of the central fixation. Together this promoted the filtering of task-irrelevant interference by the eye stimuli and facilitated target detection (Desimone and Duncan, 1995; Pessoa, 2010; Pessoa et al., 2002a).

4.1.2. Increased Activity in Cognitive Control and Attentional Neural Networks are