Two electrophysiological stages of spatial orienting towards fearful faces: Early temporo-parietal activation preceding gain control in extrastriate visual cortex Gilles Pourtois, a, T Gregor Thut, b Rolando Grave de Peralta, b Christoph Michel, b and Patrik Vuilleumier a,c a Department of Neuroscience, Neurology and Imaging of Cognition, Clinic of Neurology, University Medical Centre (CMU), Bat. A, Physiology, 7th Floor, Room 7042, 1 rue Michel-Servet, CH-1211 Geneva, Switzerland b The Functional Brain Mapping Laboratory, Neurology Clinic, Switzerland c Department of Psychology, University of Geneva, Switzerland Received 19 August 2004; revised 16 December 2004; accepted 11 January 2005 Available online 2 March 2005 Visuo-spatial attention tends to be prioritized towards emotionally negative stimuli such as fearful faces, as opposed to neutral or positive stimuli. Using a covert orienting task, we previously showed that a lateral occipital P1 component, with extrastriate neural sources, was selectively enhanced to lateralized visual targets replacing a fearful face (fear-valid trial) than the same targets replacing a neutral face (fear-invalid trial), providing evidence for exogenous spatial orienting of attention towards threat cues. Here, we describe a new analysis of these data, using topographic evoked potentials mapping methods combined with a distributed source localization technique. We show that an early field topography (40–80 ms post-target onset) with a centro- parietal negativity and a left posterior parietal source distinguished fear-valid from fear-invalid trials, whereas a distinct activity with anterior cingulate sources was selectively evoked during fear- invalid trials. At the same latency, or later, no difference in field topography was found for valid compared to invalid trials with happy faces. The early parietal map preceded a modulation in amplitude of the field strength (~130ms), corresponding to the enhanced lateral occipital P1 during valid trials in the fear condition. Furthermore, this early topography at 40–80 ms was positively correlated with the subsequent amplitude modulation of P1 at 130–160 ms in the fear condition, suggesting a possible functional coupling between these two successive events. These data have important implications for models of spatial attention and interactions with emotion. They suggest two successive stages of neural activity during exogenous orienting of attention towards visual targets following fearful faces, including an early posterior parietal negativity, followed by gain control mechanisms enhancing visual responses in extrastriate occipital cortex. D 2005 Elsevier Inc. All rights reserved. Keywords: Fear; Covert orienting; Temporal segmentation; Spatial clustering; Distributed source localization; Posterior parietal cortex; Anterior cingulate cortex; Feedback; Gain control mechanism Introduction The brain response to sensory stimuli is strongly modulated by endogenous mechanisms such as spatial attention, as well as by emotional factors. Spatially orienting attention to a stimulus allows selective perceptual processing (Luck, 1995; Luck et al., 2000), usually attributed to top–down control from fronto-parietal cortical areas (e.g., Corbetta and Shulman, 2002; Hopfinger et al., 2000). Numerous behavioral studies have shown that attention is also more readily drawn to emotionally negative than to neutral stimuli (Anderson and Phelps, 2001; Bradley et al., 1997; sometimes with variable hemispheric effects, e.g., Hartikainen et al., 2000), suggesting an additional modulation by emotional processes (Amaral et al., 2003; Vuilleumier, 2002). Consistent with this, functional neuroimaging studies have found increased neural activation in both visual (Lane et al., 1998; Lang et al., 1998; Vuilleumier et al., 2001) and fronto-parietal areas (Armony and Dolan, 2002; Fredrikson et al., 1995) for threat-related compared to neutral visual events. These findings converge to suggest that behaviorally significant stimuli can promote deeper processing at early stages of sensory pathways due to the joint influence of attentional and emotional mechanisms. Such a modulation of extrastriate visual areas implies that specific neural processes need to be activated at a prior stage to 1053-8119/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2005.01.015 T Corresponding author. Fax: +41 22 379 5402. E-mail address: gilles.pourtois@medecine.unige.ch (G. Pourtois). Available online on ScienceDirect (www.sciencedirect.com). www.elsevier.com/locate/ynimg NeuroImage 26 (2005) 149 – 163