Endogenous and exogenous attention shifts are mediated by the same large-scale neural network Marius V. Peelen, Dirk J. Heslenfeld, * and Jan Theeuwes Department of Psychology, Vrije Universiteit, Amsterdam, The Netherlands Received 16 October 2003; revised 24 December 2003; accepted 24 January 2004 Available online 14 April 2004 Event-related fMRI was used to examine the neural basis of endogenous (top-down) and exogenous (bottom-up) spatial orienting. Shifts of attention were induced by central (endogenous) or peripheral (exogenous) cues. Reaction times on subsequently presented targets showed the expected pattern of facilitation and inhibition in both conditions. No difference in brain activity was observed when the two orienting conditions were contrasted with a liberal threshold, showing that both forms of orienting were mediated by the same neural network. Compared to within-block control trials, both endogenous and exogenous orienting activated a fronto-parietal network consisting of premotor cortex, posterior parietal cortex, medial frontal cortex and right inferior frontal cortex. Within these regions, equally strong activation was observed for both orienting conditions. It is concluded that endogenous and exogenous orienting are mediated by the same large-scale network of frontal and parietal brain areas. D 2004 Published by Elsevier Inc. Keywords: Visual Attention; Spatial orienting; Functional MRI; Event- related fMRI; Endogenous; Exogenous; Human Introduction An important question in attention research is how attention is allocated in visual space. Generally, a distinction is made between two types of attentional orienting: endogenous and exogenous orienting (Jonides, 1981). Endogenous or top-down orienting refers to the controlled, voluntary allocation of attention. Exoge- nous or bottom-up orienting refers to the automatic, involuntary allocation of attention. A frequently used paradigm to study endogenous and exogenous orienting is Posner’s cueing paradigm (Posner, 1980; Posner and Cohen, 1984). Subjects have to respond as fast as possible to a peripheral target, which is preceded by a central or peripheral cue. In the endogenous orienting condition, a central cue (typically an arrow) points to the most likely location of the subsequent target. Typically, the time to respond to targets presented at the cued location is shorter than the time to respond to targets presented at the uncued location, suggesting that attention was endogenously shifted to the cued location. In an exogenous orienting condition, typically a brief peripheral onset cue is presented at one of the target locations. The cue is not predictive about the location of the subsequent target and it is assumed that the cue attracts attention automatically. Similar to central cueing, subjects are faster in responding to targets presented at the cued location than at the uncued location. However, unlike in central cueing, when the stimulus onset asynchrony (SOA) between cue and target exceeds approximately 250 ms, subjects respond slower to targets presented at the cued location (Klein, 2000; Posner and Cohen, 1984). This phenomenon, called inhibition of return (IOR), occurs only in typical exogenous orienting conditions. Note that although peripheral cueing does not preclude endogenous attention shifts, and central cueing may not preclude exogenous attention shifts, their relative contribution may be expected to be small given the types of cues and their predictive values. Research on monkeys and neurological patients has revealed that the two forms of orienting may be mediated, at least in part, by different neural structures. Patients with lesions in the superior colliculus (SC), as in progressive supranuclear palsy, have diffi- culty with exogenous but not endogenous orienting (Rafal and Henik, 1994; Rafal et al., 1988). Research on macaque monkeys also showed that the SC is involved in exogenous orienting (Milner et al., 1978; Robinson and Kertzman, 1995) but not in endogenous orienting (Robinson and Kertzman, 1995). In contrast, patients with lesions in the temporo-parietal junction (TPJ), including superior temporal gyrus, have difficulty interpreting endogenous cues, but their attention can be attracted by peripheral onsets (Rafal and Henik, 1994). Contrary to this finding, recent studies on left unilateral neglect patients, often resulting from lesions to or near to the TPJ, show a specific deficit in exogenous orienting (Bartolo- meo and Chokron, 2002; Bartolomeo et al., 2001). Further support for a role of the TPJ in exogenous orienting comes from an fMRI study by Corbetta et al. (2000). They showed that the TPJ is strongly activated when a peripheral target is detected, in particular when it is presented at an unattended location. The aim of the present study was to compare in detail the neural architecture of endogenous and exogenous orienting in healthy humans by using event-related fMRI. Previous imaging studies reported both large overlap and differences in brain activity 1053-8119/$ - see front matter D 2004 Published by Elsevier Inc. doi:10.1016/j.neuroimage.2004.01.044 * Corresponding author. Department of Cognitive Psychology, Vrije Universiteit, van der Boechorststraat 1, 1081 BT Amsterdam, The Netherlands. Fax: +31-20-444-8832. E-mail address: dirk@psy.vu.nl (D.J. Heslenfeld). Available online on ScienceDirect (www.sciencedirect.com.) www.elsevier.com/locate/ynimg NeuroImage 22 (2004) 822 – 830