Modulation of attentional blink with emotional faces in typical development and in autism spectrum disorders.

Attention capacity is limited, but emotionally significant information can overcome this limitation to capture attention. This is demonstrated in the auditory domain by the well-known “cocktail party” effect, where we notice our name, but not much else in another group’s conversation. In the visual domain, the attentional blink (AB) phenomenon is abolished or reduced for emotional stimuli. AB refers to unawareness of a second target (Target2) presented immediately (e.g., 200–400ms) but not later (e.g., 600 ms) after identifying the first target (Target1). This lapse in perceptual awareness immediately following target identification is akin to a “blink”, and is thought to reflect limitations in attention resources; resources are momentarily depleted immediately following their engagement in the identification of Target1 and recover over time (Fox, Russo, & Georgiou, 2005). However, emotionally significant Target2 stimuli (e.g., emotionally arousing words, like “NAKED”) reduce or abolish the AB effect; emotional Target2 stimuli are perceived with greater accuracy than neutral Target2 stimuli immediately after identification of Target1 (Anderson, 2005). The AB paradigm, therefore, examines the influence of encoding emotional information implicitly; that is, encoding without requiring explicit evaluation of emotional valence. Reduction of the AB effect with emotional information indicates that emotional valence influences early visual attention. Prior brain imaging and neuropsychological studies suggest that testing emotional information processing in early visual attention is an assay of amygdala function. Structural imaging studies of human and non-human primates showed that the amygdala has direct connections with cortical (prefrontal cortex) and subcortical (pulvinar) areas that are involved in visual attention (Adolphs, 2003; Amaral, Price, Pitkanen, & Carmichael, 1992; Pessoa & Adolphs, 2010). Bilateral lesions to the amygdala led to impaired recognition of fearful facial expressions (Adolphs, Tranel, Damasio, & Damasio, 1994). Adults with post-traumatic stress disorder, a disorder characterized by atypical amygdala function, showed an enhanced amygdala response when disengaging attention from threatening faces (El Khoury-Malhame et al., 2011). The AB effect for emotional information depends upon the amygdala as adults with bilateral amygdala damage failed to show a reduced AB effect for emotional words (Anderson & Phelps, 2001). Thus, bilateral amygdala damage eliminated privileged access to emotional information in early visual attention. Functional neuroimaging studies of the AB effect showed that increased amygdala activation correlated with a reduced AB effect for emotional stimuli, providing direct evidence that the amygdale mediates emotional modulation of the AB effect (Lim, Padmala, & Pessoa, 2009). Sensitivity of the emotional AB effect to amygdala damage in neuropsychological patients and amygdala engagement in healthy individuals supports its use as an assay for contributions of the amygdala to early visual attention. Histologic and neuroimaging evidence documents altered amygdala development and function in ASD (Amaral, Schumann, & Nordahl, 2008); this alteration is posited to underlie core social impairments in ASD (Dawson, Webb, & McPartland, 2005; Schultz, 2005). Tasks assessing core social impairments can be parsed into two categories: explicit evaluation of emotional information (‘explicit’) vs. implicit encoding of emotional information (‘implicit’). Most behavioral studies in the ASD literature have used explicit tasks that require direct comparison of facial expressions or pairing expressions with emotional words. Adults and children with ASD have difficulty with facial expression recognition (Boraston, Blakemore, Chilvers, & Skuse, 2007; Davies, Bishop, Manstead, & Tantam, 1994; Gross, 2008; Hobson, 1986; Macdonald et al., 1989; Tardif, Laine, Rodriguez, & Gepner, 2007), but this is not a universal finding (see Harms, Martin, & Wallace, 2010 for comprehensive view). In comparison, few ASD studies outside of the neuroimaging environment have used implicit tasks. Adults with ASD demonstrated an intact AB effect with neutral words, but failed to show a reduced AB effect for identifying emotional words (Corden, Chilvers, & Skuse, 2008; Gaigg & Bowler, 2009), indicating that early visual attention is selectively disrupted for emotional information. In contrast, adults with ASD showed an intact spatial attention bias to faces with emotional expressions (Monk et al., 2010). Based on these findings, it is not possible to discern whether impairment of implicit emotional processing in ASD is selective to stimuli (words rather than pictures) or attentional process (visual perception rather than spatial attention). The present study examined the emotional modulation of the AB effect in 8–14 year-old children with and without ASD. It is important to investigate this effect in ASD children for two reasons: First, there are no published studies of implicit emotional processing in early visual attention in ASD children. In typical development, electrophysiological evidence indicates that visual processing of emotional faces becomes more efficient with age (Batty & Taylor, 2006) and voluntary attention (indexed by P300) is higher for angry than happy faces for children but was higher for happy than angry faces for adults (Kestenbaum & Nelson, 1992). If such developmental differences are paralleled in ASD, it is possible that the emotional AB effect differs between ASD adults and children. Second, explicit identification of emotion in faces was worse in adults with ASD than controls but this finding did not extend to school age children and adolescents (Rump, Giovannelli, Minshew, & Strauss, 2009). If this developmental difference is paralleled in implicit emotional processing, AB findings from ASD adults may not extend to ASD children. In the 8 to 14 age range children are sensitive to emotional faces, such as anger (Barnes, Kaplan, & Vaidya, 2007). Thus, this is an important period for examining implicit emotional processing. Our AB paradigm used picture stimuli, headshots of dogs as Target1 and faces with neutral or angry expressions as Target2. We used target pictures rather than words, because language impairments are common in ASD and we wanted to limit their effect on performance. Further, the emotional targets were faces with angry expressions because past findings show that the AB associated with angry faces is more robust than that associated with happy faces (Maratos, 2011)