The timing and directional connectivity of human frontoparietal and ventral visual attention networks in emotional scene perception
Introduction
Electrocortical and hemodynamic measures reveal enhanced activity in ventral and dorsal visual cortices during emotional relative to neutral picture perception (Pourtois et al., 2004, Sabatinelli et al., 2005, Pessoa et al., 2006, Anticevic et al., 2011, Sabatinelli et al., 2013, Wiens and Syrjanen, 2013), an effect that may reflect a natural selective attention to behaviorally relevant stimuli (Vuilleumier and Driver, 2007, Lang and Bradley, 2010, Pessoa and Adolphs, 2010, Markovic et al., 2013). Some evidence suggests an association between enhanced fusiform gyrus (FG) activity and directive feedback from the subcortical amygdala (Armony and Dolan, 2002, Vuilleumier et al., 2004, Sabatinelli et al., 2005, Sabatinelli et al., 2009).
However, other brain regions strongly modulate visual attention, such as frontal eye fields (FEF) and intraparietal sulcus (IPS) (Rizzolatti et al., 1987, Corbetta, 1998, Schafer and Moore, 2007, Bisley and Goldberg, 2010). This frontoparietal (FP) network is persistently involved in a process of categorizing stimulus relevance and directing the locus of visual attention (Corbetta et al., 2008). While the characteristics of this FP network have been thoroughly investigated in target-driven visuospatial attention tasks (Serences and Yantis, 2006) the role of stimulus emotion on the engagement of this network is underexplored. While studies have demonstrated that emotional stimuli evoke augmented FP activity (Moratti et al., 2004, Sabatinelli et al., 2007a, Sabatinelli et al., 2007b, Shafer and Dolcos, 2012, Brosch and Grandjean, 2013, Ferri et al., 2013), the mechanisms by which emotional characteristics modulate FP activity are poorly defined (Adolphs, 2002, Mitchell et al., 2008, Vuilleumier and Huang, 2009, Frank and Sabatinelli, 2012).
One means of addressing research questions regarding the temporal order of human brain activity is through comparisons of the relative timing of the BOLD signal within a structure across experimental conditions. While the BOLD signal is inherently delayed and smoothed relative to neural activity, the timing of signal change within active clusters is highly reliable (Kim et al., 1997, Menon and Kim, 1999, Miezin et al., 2000, Lin et al., 2013). Here we sample the BOLD contrast four times per second in 4-slice slabs of ventral (amygdala and FG) and dorsal (FEF and IPS) brain regions during an emotional and neutral picture series to test whether emotional discrimination is apparent in the FP network prior to such emotional discrimination in the amygdala and FG. There is evidence for a rapid response latency in human (Kirchner et al., 2009) and macaque (Schmolesky et al., 1998) FEF, and human data that suggest a role for FEF in modulating attention enhancement in the visual cortex (Taylor et al., 2007). If picture stimulus emotion is discriminated in the FP network prior to the amygdala and FG, a reentrant perspective of emotional perception (Freese and Amaral, 2005, Sabatinelli et al., 2009, Vuilleumier and Huang, 2009) would not be supported. If emotional discrimination is apparent in the amygdala and FG prior to such discrimination in the FP network, the emotionally-enhanced activity seen in FP structures during scene perception may reflect input from the amygdala and FG, or other regions not yet sampled.
Rapid sampling also provides an opportunity to determine potential asymmetries in directional connectivity between structures within the ventral and dorsal networks using Granger connectivity analyses. As there is support for a directive effect of the amygdala on FG (Anderson and Phelps, 2001, Vuilleumier and Driver, 2007, Sabatinelli et al., 2009) and for the FEF on IPS (Bressler et al., 2008), the current data will enable a test of these hypothesized directional connectivities in an emotional picture perception task.
Section snippets
Participants and procedure
Forty-five undergraduate students from the University of Georgia participated in the experiment, receiving $20 USD compensation. Three subjects’ data were lost due to MR scanner or stimulus presentation equipment malfunction. Of the 42 participants (average age 22 years, standard deviation (SD) 3) in the final sample, 20 were female. All participants gave informed consent, and this study was approved by the University of Georgia Human Subjects Review Board. All participants reported no
Stimulus ratings
Averages and standard errors of valence and arousal ratings for the 80 picture stimuli used in this study are shown in Table 1. The ratings for the 20 picture stimuli selected from the International Affective Picture System (IAPS) are drawn from the normative values (also drawn from undergraduate sample) published in the IAPS technical manual (Lang et al., 2008), and differed reliably across valence (F (2, 17) = 69.00, p < .001) with pleasant stimuli yielding higher valence ratings relative to
Discussion
Assessing the relative contributions of dorsal and ventral structures to the process of emotional discrimination in humans is methodologically challenging, as high levels of spatial and temporal resolution are necessary, and direct access to all structures of interest via invasive methods is extremely rare. Moreover, ventromedial cortical and subcortical regions present a particularly weak signature in the noninvasive electro- and magneto-encephalogram. One means of addressing the research
Study limitations
Our primary goal in this experiment was to determine if the emotional discrimination we knew to exist in the FP network preceded such discrimination in the amygdala and FG. While it may be tempting to interpret the relative timing of emotional discrimination as suggesting a hierarchy from ventral to dorsal structures, the current data cannot speak of this relationship directly, as these regions were sampled at different times. Moreover, GC analyses were performed to address separate questions
Conflict of interest
The authors declare no competing financial interests.
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