Human Frontal Eye Fields and Spatial Priming of Pop-out Jacinta O’Shea1, Neil G. Muggleton2, Alan Cowey1, and Vincent Walsh2 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/19/7/1140/1756786/jocn.2007.19.7.1140.pdf by guest on 18 May 2021 Abstract & ‘‘Priming of pop-out’’ is a form of implicit memory that a saccade is being programmed to a repeated target color facilitates detection of a recently inspected search target. Re- or location, TMS was applied during the search array. TMS peated presentation of a target’s features or its spatial position over the left but not the right FEFs abolished spatial priming, improves detection speed (feature/spatial priming). This study but had no effect on feature priming. These findings dem- investigated a role for the human frontal eye fields (FEFs) in onstrate functional specialization of the left FEFs for spatial the priming of color pop-out. To test the hypothesis that the priming, and distinguish this role from target discrimination FEFs play a role in short-term memory storage, transcranial and saccade-related processes. The results suggest that the magnetic stimulation (TMS) was applied during the intertrial left FEFs integrate a spatial memory signal with an evolving interval. There was no effect of TMS on either spatial or fea- saccade program, which facilitates saccades to a recently in- ture priming. To test whether the FEFs are important when spected location. & INTRODUCTION control, this paradigm eliminates task strategy complica- ‘‘Priming of pop-out’’ (PoP) describes the detection tions from the effort to dissociate memory mechanisms benefit (speed/accuracy) that accrues when an observer from search and saccade-related processes. searches repeatedly for the same odd-one-out target (e.g., In a functional magnetic resonance imaging (fMRI) red) among the same distractors (e.g., green), com- study, Kristjansson, Vuilleumier, Schwartz, Macaluso, and pared with the cost when the target–distractor combi- Driver (2006) (see also Yoshida, Tsubomi, Osaka, & Osaka, nations change across trials (Maljkovic & Nakayama, 2003) found that repetition of a target’s features or loca- 1994, 1996). If the target on the current trial has the tion induced bilateral suppression of blood oxygen level- same features or spatial location as the target on the dependent (BOLD) signal in the frontal eye fields (FEFs) previous trial, detection is faster. Manual and saccadic and a number of parietal regions (including the angular reaction time (RT) benefits of up to 50 msec have been gyrus [AG]). Feature priming induced additional sup- demonstrated in both humans and monkeys (McPeek & pression in infero-temporal areas involved in color pro- Keller, 2001; McPeek, Maljkovic, & Nakayama, 1999). cessing. Repetition suppression is believed to reflect Priming has been attributed to ‘‘a decaying memory reduced neuronal discharge on repeated stimulus pre- trace’’ of the search target that is laid down on each sentation and has been shown to correlate with priming trial. It is proposed to reflect an implicit memory sys- in a variety of paradigms (Henson & Rugg, 2003; Kourtzi tem that is specialized for rapid, automatic target selec- & Kanwisher, 2000; Wiggs & Martin, 1998; Desimone, tion for saccades (Maljkovic & Nakayama, 2000). One 1996). One question posed by these fMRI data is wheth- challenge is to disentangle the mechanisms in fronto- er fronto-parietal repetition suppression is task-critical. parietal cortex that appear to be common to search, Because FEF neurons are not color-selective (Mohler, eye movements, and spatial working memory (LaBar, Goldberg, & Wurtz, 1973), they would not be expected Gitelman, Parrish, & Mesulam, 1999; Corbetta et al., to mediate color priming. Nevertheless, it has been 1998). Tonic neural activity in the delay period of spa- shown that color priming modulates FEF activity. Bichot tial working memory tasks has been shown to reflect and Schall (2002) recorded from FEF visuomovement visual, mnemonic, and oculomotor signals (Curtis & neurons and showed that on color-repeat trials, target D’Esposito, 2006; Sommer & Wurtz, 2001). Because selection activity developed earlier, and there was a PoP is passive, automatic, and not subject to conscious greater difference between target- and distractor-related activity in the post-selection period. These effects seem best interpreted as downstream influences of adapta- 1University of Oxford, UK, 2University College London, UK tion in sensory visual cortex. Much evidence suggests D 2007 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 19:7, pp. 1140–1151 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2007.19.7.1140 by guest on 26 September 2021 that the cortical visual areas selective for a particular fea- ment, and spatial memory tasks (Chafee & Goldman- ture (e.g., color) also support perceptual memory for Rakic, 1998, 2000). During search tasks, patients with that feature (Tulving & Schacter, 1990). Three studies right parietal lesions frequently return to previously in- have shown that V4 lesions abolish color PoP (Girard, spected items and show no awareness of having done so Choitel, & Bullier, 2001; Rossi, Bichot, Desimone, & (Pisella, Berberovic, & Mattingley, 2004; Husain et al., Ungerleider, 2001; Walsh, Le Mare, Blaimire, & Cowey, 2001). This ‘‘revisiting’’ behavior has been interpreted as 2000). Even after complete removal of the unilateral pre- a failure to maintain or update searched locations across frontal cortex, the corpus callosum, and the anterior saccades. Revisiting behavior has been argued to de- commissure, Rossi et al. showed that color PoP re- pend on damage to the right AG and/or the intraparietal Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/19/7/1140/1756786/jocn.2007.19.7.1140.pdf by guest on 18 May 2021 mained unaffected. Collectively, these studies suggest sulcus (Mannan et al., 2005), but monkeys with FEF (but that color priming requires intact V4, and that repetition not superior colliculus) lesions also show revisiting be- suppression in the FEFs reflects changes in the effi- havior (Collin, Cowey, Latto, & Marzi, 1982). The data on ciency of target selection, but that these depend on ‘‘revisiting’’ behavior would predict that AG lesions or sensory adaptation in color-selective cortex. TMS should disrupt spatial PoP. However, to our knowl- There are reasons to expect that spatial priming may edge, only one study has tested right parietal patients require a causal contribution from the FEFs. Whereas on implicit spatial memory using color PoP. Kristjansson changes in target selection activity in FEF visual neurons et al. (2005), using manual responses, reported that both can be considered in terms of a ‘‘visual salience map,’’ feature and spatial priming were intact in both of their spatial priming can also be conceptualized as maintain- patients who had neglect and extinction. Spatial priming ing or switching task set (Fecteau & Munoz, 2003). When occurred as long as the patient had detected the target the same saccade program must be re-executed (‘‘stay’’ on the previous trial, but feature priming occurred irre- trials), performance is easier than when a new saccade spective of prior target detection. Hence, the role of the must be programmed (‘‘switch’’ trials). Thus, spatial prim- AG in spatial PoP requires further investigation. ing may be thought of as a form of oculomotor mem- The central aim of the present study was to investigate ory. By contrast with the spatial PoP paradigm, cueing whether the FEFs make causal contributions to feature paradigms have reported ‘‘inhibition of return,’’ a slow- or spatial PoP with saccadic responses. We hypothesized ing of saccadic responses when a target location is pre- that TMS applied over the FEFs would disrupt spatial but cued (for a review, see Klein, 2000). Both facilitation not feature priming. In addition, we investigated a poten- and inhibition effects can be measured in a PoP para- tial role for the AGs in spatial priming. Because the AGs digm, but target-position facilitation appears to always be form a functionally integrated circuit with the FEFs during stronger than distractor-position inhibition (Maljkovic & tasks that require visual search, target selection, saccade Nakayama, 1996). Consistent with this, PoP studies almost programming, and spatial memory, we expected some unanimously report facilitation at the primed location interference at both TMS sites. Hence, we asked whether (e.g., Kristjansson et al., 2006; Kristjansson, Vuilleumier, any such effects might dissociate across timing condi- Malhotra, Husain, & Driver, 2005; McPeek et al., 1999). tions, or whether the FEFs or the AGs might have a dom- Saccadic priming has been shown to correlate with inant role. To test for a role in primed memory storage changes in the baseline firing rate of superior colliculus across trials, TMS was applied in the intertrial interval neurons, altering the threshold for saccade initiation (ITI). To test whether the FEFs are important when a (Gore, Dorris, & Munoz, 2002; Dorris, Pare, & Munoz, saccade is repeated toward a primed feature or location, 2000). Location switch costs have also been ascribed to TMS was applied during presentation of the search array. competing oculomotor programs within the superior col- Four experiments were conducted, with controls for task liculus (McPeek, Han, & Keller, 2003; McPeek & Keller, (feature/spatial), TMS site (FEFs/AGs), hemisphere (left/ 2002).