ffective learning enhances activity and functional connectivity in arly visual cortex

This study examined the impact of task-irrelevant affective information on early visual processing regions V1–V4. Fearful and neutral faces presented with rings of different colors were used as stimuli. During the conditioning phase, fearful faces presented with a certain ring color (e.g., black) were paired with mild electrical stimulation. Neutral faces shown with rings of that color, as well as fearful or neutral faces shown with another ring color (e.g., white), were never paired with shock. Our findings revealed that fearful faces evoked enhanced blood oxygen level dependent (BOLD) responses in V1 and V4 compared to neutral faces. rimary visual cortex onditioning aces ision motion MRI Faces embedded in a color ring that was paired with shock (e.g., black) evoked greater BOLD responses in V1–V4 compared to a ring color that was never paired with shock (e.g., white). Finally, BOLD responses in early visual cortex were tightly interrelated (i.e., correlated) during an affectively potent context (i.e., ring color) but not during a neutral one, suggesting that increased functional integration was present with affective learning. Taken together, the results suggest that task-irrelevant affective information not only influences evoked responses in early, retinotopically organized visual cortex, but also determines cross the pattern of responses a Accumulating evidence shows that the processing of affecively significant visual objects is prioritized (Compton, 2003; uilleumier, 2005). Affective stimuli that have dominance in visual wareness (Alpers & Gerdes, 2007; Alpers & Pauli, 2006) are proessed faster (Stolarova, Keil, & Moratti, 2006) and are more likely to e processed when only limited resources are available (Anderson, 005; Anderson & Phelps, 2001). Neuroanatomical connections etween orbitofrontal cortex (OFC) and both the ventral and doral visual streams (Barbas, 1988, 1995; Carmichael & Price, 1995; avada, Company, Tejedor, Cruz-Rizzolo, & Reinoso-Suarez, 2000), s well as projections from the amygdala all along the ventral tream (Amaral, Behniea, & Kelly, 2003; Amaral, Price, Pitkänen, & armichael, 1992), suggest that affective brain regions functionally odulate visual processing regions (Barrett & Bar, 2009; Duncan Barrett, 2007; Lang et al., 1998; Pessoa & Ungerleider, 2004; uilleumier, 2005). There is accumulating neuroimaging evidence hat objects with affective value receive enhanced visual processng even in early, retinotopically organized cortex (e.g., V1–V4). oth affectively salient images (Lane, Chua, & Dolan, 1999; Lang et l., 1998; Mourão-Miranda et al., 2003) and faces (Büchel, Morris, olan, & Friston, 1998; Vuilleumier, Richardson, Armony, Driver, & olan, 2004) evoke enhanced blood oxygen level dependent (BOLD) ∗ Corresponding author. E-mail address: yangming.huang@gmail.com (Y.-M. Huang). 028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. oi:10.1016/j.neuropsychologia. 2009.04. 023 early visual cortex. © 2009 Elsevier Ltd. All rights reserved. responses in early visual areas. A recent meta-analytic investigation summarizing functional magnetic resonance imaging (fMRI) and PET studies of emotion published from 1990 to 2005 confirmed that visual processing areas are consistently activated in response to affectively potent as compared with neutral stimuli (Kober et al., 2008; see Fig. 2 in Wager et al., 2008). Recent studies have examined how learning the association between a neutral stimulus and electrical stimulation affects associated responses in early sensory areas more generally. For instance, Li, Howard, Parrish, and Gottfried (2008) reported that pairing an odor with electrical stimulation changed the pattern of activity in primary olfactory cortex and enabled participants to discriminate previously indiscriminable odors. In a related study, Padmala and Pessoa (2008) paired the presence of a near-threshold visual patch with electrical stimulation during an initial conditioning phase. In a subsequent experimental phase, participants were better at detecting the visual stimulus when it was predictive of electrical stimulation, a result that was paralleled by increased signal changes in V1, as well as other retinotopically organized visual areas. Related studies have capitalized on the fine temporal resolution of EEG to address analogous questions (e.g.,Keil, Stolarova, Moratti, & Ray, 2007; Schupp, Junghöfer, Weike, & Hamm, 2003). However, several properties of the impact of affective learning on early sensory representations remain poorly understood. For instance, in previous studies, the effect of learning on sensory representations was typically evaluated for stimuli that are E. Damaraju et al. / Neuropsychol Fig. 1. The experimental design contained four face-ring stimuli combinations. D u c F b l t a i & a i l i o f b i r i f f w a